Skip to main content
Log in

Basement-membrane components associated with the extracellular matrix of the lymph node

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Lymph nodes contain an extensive array of extracellular matrix fibers frequently referred to as “reticular fibers” because of their reticular pattern and positive reaction with silver stains. These fibers are known to contain primarily type-III collagen. In the present study, frozen and plastic-embedded sections of mouse and human lymph nodes were subjected to immunostaining with a panel of monospecific antibodies directed against type-IV collagen, type-III collagen, laminin, entactin, and heparan sulfate proteoglycan. Immunofluorescent staining revealed that, in addition to being uniformly stained with antibodies to type-III collagen, these fibers also stained positively with antibodies to type-IV collagen and to other basement-membrane-specific components. Furthermore, the basement-membrane-specific antibodies stained the outer surface of individual fibers. These same type-III collagen-rich fibers were distinct from blood vascular basement membranes since they did not react with antibodies to factor VIII-related antigen, an endothelial-cell-specific marker. The role of these basement-membrane-specific components associated with the reticular fibers of lymphoid tissue is unknown. However, it is possible that the ligands promote attachment of reticular fibroblasts as well as macrophages and lymphocytes to the extracellular matrix fibers.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abrahamson DR (1986) Recent studies on the structure and pathology of basement membranes. J Pathol 149:257–278

    Google Scholar 

  • Amenta PS, Gay S, Vaheri A, Martinez-Hernandez A (1986) The extracellular matrix is an integrated unit: Ultrastructural localization of collagen type I, III, IV, V, and VI, fibronectin, and laminin in human term placenta. Coll Rel Res 6:125–152

    Google Scholar 

  • Bachinger HP, Flessler LI, Flessler JH (1982) Mouse procollagen IV: characterization and supramolecular association. J Biol Chem 257:9796–9803

    Google Scholar 

  • Bairati A, Amantie L, de Petris S, Pernis B (1964) Studies on the ultrastructure of the lymph nodes. 1. The reticular network. Z Zellforsch 63:644–672

    Google Scholar 

  • Barsky SH, Baker A, Siegal GP, Togo S, Liotta LA (1983) Use of anti-basement-membrane antibodies to distinguish blood vessel capillaries from lymphatic capillaries. Am J Surg Pathol 7:667–677

    Google Scholar 

  • Becker U, Nowack H, Gay S, Timpl R (1976) Production and specificity of antibodies against the aminoterminal region in type III collagen. Immunology 31:57–65

    Google Scholar 

  • Beckstead JH (1983) The evaluation of human lymph nodes, using plastic sections and enzyme histochemistry. Am J Clin Pathol 80:131–139

    Google Scholar 

  • Beckstead JH, Wood GS, Fletcher V (1985) Evidence for the origin of Kaposi's sarcoma from lymphatic endothelium. Am J Pathol 119:294–300

    Google Scholar 

  • Burgeson RE (1982) Genetic heterogeneity of collagens. J Invest Dermatol 79:25s-30s

    Google Scholar 

  • Chen L-T, Weiss L (1972) Electron microscopy of the red pulp of the human spleen. Am J Anat 134:425–458

    Google Scholar 

  • Clark SL, Jr (1962) The reticulum of lymph nodes in mice studied with the electron microscope. Am J Anat 110:217–258

    Google Scholar 

  • Drenckhahn D, Wagner J (1986) Stress fibers in the splenic sinus endothelium in situ: Molecular structure, relationship to the extracellular matrix, and contractility. J Cell Biol 102:1738–1747

    Google Scholar 

  • D'Ardenne AJ, Burns J, Sykes BC, Kirkpatrick P (1983) Comparative distribution of fibronectin and type III collagen in normal human tissues. J Pathol 141:155–169

    Google Scholar 

  • Ewenstein BM, Warhol HL, Handin RI, Pober JS (1987) Composition of the von Willebrand factor storage organelle (Weibel-Palade body) isolated from cultured human umbilical vein endothelial cells. J Cell Biol 104:1423–1433

    Google Scholar 

  • Farquhar MG (1978) Structure and function in glomerular capillaries: role of the basement membrane in glomerular filtration. In: Kefalides, NA (ed.) Biology and Chemistry of Basement Membranes. Academic Press, New York, NY

    Google Scholar 

  • Forkert P-G, Thliveris JA, Bertalanffy FD (1977) Structure of sinuses in the human lymph node. Cell Tissue Res 183:115–130

    Google Scholar 

  • Fossum S (1980) The architecture of rat lymph nodes. II. Lymph node compartments. Scand J Immunol 12:411–420

    Google Scholar 

  • Freemont AJ, Stoddart RW, Steven F, Jones CJ, Matthews S (1986) The structure of the basement-membrane of human lymph node high endothelial venules: an ultrastructural, histochemical and immunocytochemical study. Histochem J 18:421–428

    Google Scholar 

  • Fresen F, Wellensiek RB (1959) Zur elektronoptischen Struktur des Lymphknotens. Verh Dtsch Ges Pathol 42:353–363

    Google Scholar 

  • Gridley MF (1951) A modification of the silver impregnation method of staining reticular fibers. Am J Clin Pathol 21:897–899

    Google Scholar 

  • Hassel JR, Robey RB, Barrach HJ, Wilczek J, Rennard SI, Martin GR (1980) Isolation of heparan sulfate proteoglycan-containing proteoglycan from basement-membrane. Proc Natl Acad Sci USA 77:4494–4498

    Google Scholar 

  • Heathcote JG, Grant ME (1981) The molecular organization of basement-membranes. Int Rev Connect Tissue Res 9:191–264

    Google Scholar 

  • Hiserodt JC, Laybourn KA, Varani J (1985) Expression of a laminin-like substance on the surface of murine natural killer (NK) lymphocytes and its role in NK recognition of tumor target cells. J Immunol 135:1484–1487

    Google Scholar 

  • Hoyer LW (1981) The factor VIII complex. Structure and function. Blood 58:1–13

    Google Scholar 

  • Hynes RO (1987) Integrins: a family of cell surface receptors. Cell 48:549–554

    Article  CAS  PubMed  Google Scholar 

  • Huard TK, Malinoff HL, Wicha MS (1986) Macrophages express a plasma membrane receptor for basement membrane laminin. Am J Pathol 123:365–370

    Google Scholar 

  • Jaffe EA, Nachman RL, Becker CG, Minick GR (1973) Culture of human endothelial cells derived from umbilical cord. J Clin Invest 52:2745–2756

    CAS  PubMed  Google Scholar 

  • Junqueira LCU, Cossermelli W, Brentani R (1978) Differential staining of collagens type I, II, and III by Sirus Red and polarization microscopy. Arch Histol Jpn 41:267–274

    Google Scholar 

  • Kalimo H, Lehto M, Nanto-Salonen K, Jalkanen M, Risteli L, Risteli J, Narva EV (1985) Characterization of the perivascular reticulin network in a case of primary brain lymphoma. Immunohistochemical demonstration of collagen types I, III, IV, and V; laminin; and fibronectin. Acta Neuropathol 66:299–305

    Google Scholar 

  • Kleinman HK, Klebe RJ, Martin GR (1981) Role of collagenous matrices in the adhesion and growth of cells. J Cell Biol 88:473–485

    Google Scholar 

  • Kleinman HK, McGarvey ML, Liotta LA, Gehron-Robey P, Tryggvason K, Martin GR (1982) Isolation and characterization of type IV collagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry 21:4969–4974

    Google Scholar 

  • Kramer RH, Bensch KG, Karasek KA (1987a) Isolation and characterization of human vascular endothelial cells with application to studies of the subendothelial matrix. In: Pretlow TG, II, Pretlow TP (ed) Cell Separation: Methods and Selected Applications, Academic Press, Orlando, Vol. 5, pp 1–27

    Google Scholar 

  • Kramer RH, McDonald KA, Berston E, Damsky CH, Ramos D (1987b) Model for lymphatic metastasis: Tumor cell interaction with basement-membrane-containing reticular fibers of the lymph node. J Cell Biol 91a

  • Laurie GW, Leblond CP (1983) What is known of the production of basement membrane components. J Histochem Cytochem 31:159–163

    Google Scholar 

  • Laurie GW, Leblond CP, Martin GR (1982) Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement-membranes. J Cell Biol 95:340–344

    Google Scholar 

  • Lennert K (1978) Malignant lymphomas other than Hodgkin's disease. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Linder E, Stenman S, Lehto V-P, Vaheri A (1978) Distribution of fibronectin in human tissues and relationship to other connective tissue components. Ann NY Acad Sci 312:151–159

    Google Scholar 

  • Liotta LA, Rao CN, Barsky SH (1986) Biochemical interactions of tumor cells with the basement membrane. Annu Rev Biochem 55:1037–1057

    Google Scholar 

  • Luk SC, Nopajaroonsri C, Simon GT (1973) The architecture of the normal lymph node and hemolymph node. A scanning and transmission electron microscopic study. Lab Invest 29:258–265

    Google Scholar 

  • Macarek EJ, Howard PS, Lally ET (1986) Production and characterization of a monoclonal antibody to human type III collagen. J Histochem Cytochem 34:1003–1011

    Google Scholar 

  • Martinez-Hernandez A (1980) The hepatic extracellular matrix. I. Electron immunohistochemical studies in normal rat liver. Lab Invest 57:57–74

    Google Scholar 

  • Montes GS, Krisztan RM, Shigihara KM, Komoro R, Mourano PAS, Junqueira LCU (1980) Histochemical and morphological characterization of reticular fibers. Histochemistry 65:131–141

    Google Scholar 

  • Nopajaroonsri C, Luk SC, Simon GT (1971) Ultrastructure of the normal lymph node. Am J Pathol 65:1–24

    Google Scholar 

  • Rodin JAG (1974) Histology, A Text and Atlas. Oxford University Press, New York, pp 395

    Google Scholar 

  • Ruoslahti E, Pierschbacher MD (1986) Arg-Gly-Asp: A versatile cell recognition signal. Cell 44:517–518

    Google Scholar 

  • Sakashita S, Engval E, Ruoslahti E (1980) Basement-membrane glycoprotein laminin binds to heparin. FEBS Lett 116:243–246

    Google Scholar 

  • Sorenson GD (1960) An electron microscopic study of popliteal lymph nodes from rabbits. Am J Anat 107:73–96

    Google Scholar 

  • Stenman S, Vaheri A (1978) Distribution of a new major connective tissue protein, fibronectin, in normal human tissues. J Exp Med 147:1054–1064

    Google Scholar 

  • Stern R (1979) Experimental aspects of hepatic fibrosis. Prog Liver Dis 7:173–175

    Google Scholar 

  • Stoolman LM, Frazein A, Burton M (1985) Laminin selectively enhances the migratory activity of rodent lymphoid cells. J Cell Biol 101:259a

    Google Scholar 

  • Timpl R, Fujiwara S, Dziadek M, Aumailley M, Weber S, Engel J (1984) Laminin, proteoglycan, nidogen, and collagen IV: structural models and molecular interactions. In: Bernfield, M (ed) Basement Membranes and Cell Movement. Pitman, pp 25–36

  • Todd RB, Bowman W (1857) The physiological anatomy and physiology of man. Blanchard and Lea, Philadelphia

    Google Scholar 

  • Unsworth DJ, Scott DL, Walton KW, Walker-Smith JA, Holbrow EJ (1984) Failure of R1 type anti-reticulin antibody to react with fibronectin, collagen type III or the non-collagenous component (NCRC). Clin Exp Immunol 57:609–618

    Google Scholar 

  • Van Vliet E, Melis M, Foidart JM, Van Ewijk W (1986) Reticular fibroblasts in peripheral lymphoid organs identified by a monoclonal antibody. J Histochem Cytochem 34:883–890

    Google Scholar 

  • von der Mark K (1981) Localization of collagen types in tissues. Int Rev Connect Tissue Res 9:265–324

    Google Scholar 

  • Vracko R (1975) Basal lamina scaffold — anatomy and significance for maintenance of orderly tissue structure. Am J Pathol 77:313–346

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kramer, R.H., Rosen, S.D. & McDonald, K.A. Basement-membrane components associated with the extracellular matrix of the lymph node. Cell Tissue Res. 252, 367–375 (1988). https://doi.org/10.1007/BF00214379

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214379

Key words

Navigation