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The lymphatic system in the dorsal skinfold chamber of the Syrian golden hamster in vivo

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Abstract

The lymphatic network contributes to maintaining tissue homeostasis and immunological function by transporting fluid, plasma protein and cells from peripheral tissue via the lymph nodes into the blood vascular system. In contrast to the blood circulatory system, little is known about the lymphatic system. In particular, suitable animal models are lacking. Therefore, the dorsal skinfold chamber model was used to investigate the existence of a lymphatic system. To analyze the lymphatic network Syrian golden hamsters (n=12) fitted with titanium chambers were used. FITC-dextran of different concentrations (5% or 25%) and different molecular weights (4, 40 or 150 kDa) was used to contrast lymphatic vessels and measure initial lymph flow velocity. Intravital fluorescence microscopy enabled the quantification of diameter, velocity and branching order. Histology and electron microscopy supported the in vivo findings. Immediately after intradermal injection of FITC-dextran the lymphatics including valves were visible. The diameters of the lymphatic vessels (n=189) ranged from 133±5.4 μm (branching order 1) to 26±4.0 μm (branching order 5). Using different molecular weights of FITC-dextran, no significant differences in velocity were measured (327±157 μm/s with 4 kDa, 391±126 μm/s with 40 kDa, and 378±175 μm/s with 150 kDa). Blood and lymphatic vessels could not be differentiated clearly by H&E staining. However, endothelial cells of vessels with an irregularly shaped lumen containing no erythrocytes in cross section showed a weaker signal for CD31 staining as compared to endothelial cells of vessels containing erythrocytes. Moreover, transmission electron microscopy identified the dye-containing vessels as lymphatics after intradermal injection of Berlin Blue. In conclusion, a lymphatic network was characterized in the dorsal skinfold chamber model of the Syrian golden hamster. Thus, this well-established animal model for intravital microscopy provides the opportunity to elucidate the physiological and pathological function of the lymphatic vascular system.

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References

  1. Asaishi K, Endrich B, Götz A, Messmer K (1981) Quantitative analysis of microvascular structure and function in the amelanotic melanoma A-Mel-3. Cancer Res 41:1898–1904

    CAS  PubMed  Google Scholar 

  2. Banerji S, Ni J, Wang SX, Clasper S, Su J, Tammi R, Jones M, Jackson DG (1999) LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 144:789–801

    CAS  PubMed  Google Scholar 

  3. Bellmann S, Oden B (1959) Regeneration of surgically divided lymph vessels. Acta Chir Scand 116:99–117

    PubMed  Google Scholar 

  4. Berens von Rautenfeld D, Lubach D, Wenzel-Hora B, Klanke J, Hunneshagen C (1987) New techniques of demonstrating lymph vessels in skin biopsy specimens and intact skin with the scanning electron microscope. Arch Dermatol Res 279:327–334

    PubMed  Google Scholar 

  5. Bollinger A (1993) Microlymphatics of human skin. Int J Microcirc Clin Exp 12:1–15

    CAS  PubMed  Google Scholar 

  6. Bollinger A, Jager K, Sgier F, Seglias J (1981) Fluorescence microlymphography. Circulation 64:1195–1200

    CAS  PubMed  Google Scholar 

  7. Clark ER, Kirby-Smith HT, Rex RO, Williams RG (1930) Recent modifications in the method of studying living cells and tissues in transparent chambers inserted in the rabbit’s ear. Anat Rec 47:187

    Google Scholar 

  8. Cliff WJ, Nicoll PA (1970) Structure and function of lymphatic vessels of the bat’s wing. Q J Exp Physiol Cogn Med Sci 55:112–131

    CAS  PubMed  Google Scholar 

  9. DeFouw DO, Rizzo VJ, Steinfeld R, Feinberg RN (1989) Mapping of the microcirculation in the chick chorioallantoic membrane during normal angiogenesis. Microvasc Res 38:136–147

    CAS  PubMed  Google Scholar 

  10. Duling BR (1973) The preparation and use of the hamster cheek pouch for studies of the microcirculation. Microvasc Res 5:423–429

    CAS  PubMed  Google Scholar 

  11. Endrich B, Asaishi K, Gotz A, Messmer K (1980) Technical report—a new chamber technique for microvascular studies in unanesthetized hamsters. Res Exp Med 177:125–134

    CAS  Google Scholar 

  12. Erhard H, Rietveld FJ, Brocker EB, de Waal RM, Ruiter DJ (1996) Phenotype of normal cutaneous microvasculature. Immunoelectron microscopic observations with emphasis on the differences between blood vessels and lymphatics. J Invest Dermatol 106:135–140

    CAS  PubMed  Google Scholar 

  13. Fischer M, Franzeck UK, Herrig I, Costanzo U, Wen S, Schiesser M, Hoffmann U, Bollinger A (1996) Flow velocity of single lymphatic capillaries in human skin. Am J Physiol 270:H358–363

    CAS  PubMed  Google Scholar 

  14. Foeldi M, Kubik S (2002) Lehrbuch der Lymphologie fuer Mediziner und Physiotherapeuten. Gustav Fischer Verlag, Stuttgart

  15. Intaglietta M, Tompkins WR, Richardson DR (1970) Velocity measurements in the microvasculature of the cat omentum by on-line method. Microvasc Res 2:462–473

    CAS  PubMed  Google Scholar 

  16. Karpanen T, Egeblad M, Karkkainen MJ, Kubo H, Yla-Herttuala S, Jaattela M, Alitalo K (2001) Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 61:1786–1790

    CAS  PubMed  Google Scholar 

  17. Kobayashi H, Kawamatot S, Star RA, Waldmann TA, Tagaya Y, Brechbiel MW (2003) Micro-magnetic resonance lymphangiography in mice using a novel dendrimer-based magnetic resonance imaging contrast agent. Cancer Res 63:271–276

    Google Scholar 

  18. Kubik S, Manestar M (1995) Topographic relationship of the ventromedial lymphatic bundle and the superficial inguinal nodes to the subcutaneous veins. Clin Anat 8:25–28

    CAS  PubMed  Google Scholar 

  19. Less JR, Skalak TC, Sevick EM, Jain RK (1991) Microvascular architecture in a mammary carcinoma: branching patterns and vessel dimensions. Cancer Res 51:265–273

    CAS  PubMed  Google Scholar 

  20. Mandriota SJ, Jussila L, Jeltsch M, Compagni A, Baetens D, Prevo R, Banerji S, Huarte J, Montesano R, Jackson DG, Orci L, Alitalo K, Christofori G, Pepper MS (2001) Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 20:672–682

    PubMed  Google Scholar 

  21. Mayerson HS (1964) The physiologic importance of lymph. In: Hamilton WF (ed) Handbook of physiology. American Physiological Society, Washington DC, pp 1035–1073

  22. Menger MD, Laschke MW, Vollmar B (2002) Viewing the Microcirculation through the window: some twenty years experience with the hamster dorsal skinfold chamber. Eur Surg Res 34:83–91

    Article  PubMed  Google Scholar 

  23. Prewitt RL, Johnson PC (1976) The effect of oxygen on arteriolar red cell velocity and capillary density in the rat cremaster muscle. Microvasc Res 12:59–70

    CAS  PubMed  Google Scholar 

  24. Rusznyak I, Foeldi M, Szabo G (1969) Lymphologie—Physiologie und Pathologie der Lymphgefaesse und des Lymphkreislaufes. Gustav Fischer Verlag, Stuttgart

  25. Sauter B, Foedinger D, Sterniczky B, Wolff K, Rappersberger K (1998) Immunoelectron microscopic characterization of human dermal lymphatic microvascular endothelial cells. Differential expression of CD31, CD34, and type IV collagen with lymphatic endothelial cells vs blood capillary endothelial cells in normal human skin, lymphangioma, and hemangioma in situ. J Histochem Cytochem 46:165–176

    CAS  PubMed  Google Scholar 

  26. Skobe M, Hamber LM, Hawighorst T, Schirner M, Wolf GL, Alitalo K, Detmar M (2001) Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma. Am J Pathol 159:893–903

    CAS  PubMed  Google Scholar 

  27. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P, Riccardi L, Alitalo K, Claffey K, Detmar M (2001) Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7:192–198

    Article  CAS  PubMed  Google Scholar 

  28. Stacker SA, Caesar C, Baldwin ME, Thornton GE, Williams RA, Prevo R, Jackson DG, Nishikawa S, Kubo H, Achen MG (2001) VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 7:186–191

    Article  CAS  PubMed  Google Scholar 

  29. Stanton AW, Kadoo P, Mortimer PS, Levick JR (1997) Quantification of the initial lymphatic network in normal human forearm skin using fluorescence microlymphography and stereological methods. Microvasc Res 54:156–163

    Article  CAS  PubMed  Google Scholar 

  30. Vecchi A, Garlanda C, Lampugnani MG, Resnati M, Matteucci C, Stoppacciaro A, Schnurch H, Risau W, Ruco L, Mantovani A, et al (1994) Monoclonal antibodies specific for endothelial cells of mouse blood vessels. Their application in the identification of adult and embryonic endothelium. Eur J Cell Biol 63:247–254

    CAS  PubMed  Google Scholar 

  31. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J (2000) Vascular-specific growth factors and blood vessel formation. Nature 407:242–248

    CAS  PubMed  Google Scholar 

  32. Zweifach BW (1954) Direct observation on the mesenteric microcirculation in experimental animals. Anat Rec 120:277–291

    CAS  PubMed  Google Scholar 

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Author notes

  1. Vivien Schacht

    Present address: Molekulare Dermatologie, Universitäts-Hautklinik, Hauptstrasse 7, 79104, Freiburg, Germany

Authors and Affiliations

  1. Department of Dermatology, University of Regensburg, Germany

    Vivien Schacht & Christoph Abels

  2. Department of Functional and Applied Anatomy, Hannover Medical School, Germany

    Dirk Berens von Rautenfeld

  3. Keplerstrasse 70, 69120, Heidelberg, Germany

    Christoph Abels

Authors
  1. Vivien Schacht
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  2. Dirk Berens von Rautenfeld
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  3. Christoph Abels
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Correspondence to Christoph Abels.

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Schacht, V., Berens von Rautenfeld, D. & Abels, C. The lymphatic system in the dorsal skinfold chamber of the Syrian golden hamster in vivo. Arch Dermatol Res 295, 542–548 (2004). https://doi.org/10.1007/s00403-004-0453-8

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  • DOI: https://doi.org/10.1007/s00403-004-0453-8

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