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(American Journal of Pathology. 1999;154:385-394.)
© 1999 American Society for Investigative Pathology

Regular Articles

Angiosarcomas Express Mixed Endothelial Phenotypes of Blood and Lymphatic Capillaries

Podoplanin as a Specific Marker for Lymphatic Endothelium

Silvana Breiteneder-Geleff* , Afschin Soleiman* , Heinrich Kowalski* , Reinhard Horvat* , Gabriele Amann* , Ernst Kriehuber{dagger} , Katja Diem{ddagger} , Wolfgang Weninger{dagger} , Erwin Tschachler{dagger} , Kari Alitalo§ and Dontscho Kerjaschki*

From the Department of Clinical Pathology,* the Department of Dermatology {dagger} Division of Immunology, Allergy and Infectious Diseases, and the Department of Internal Medicine III,{ddagger} Division of Nephrology and Dialysis, University of Vienna, Vienna, Austria, and the Department of Pathology,§ Haartman Institute, Molecular/Cancer Biology Laboratory, University of Helsinki, Helsinki, Finland

Angiosarcomas apparently derive from blood vessel endothelial cells; however, occasionally their histological features suggest mixed origin from blood and lymphatic endothelia. In the absence of specific positive markers for lymphatic endothelia the precise distinction between these components has not been possible. Here we provide evidence by light and electron microscopic immunohistochemistry that podoplanin, a ~38-kd membrane glycoprotein of podocytes, is specifically expressed in the endothelium of lymphatic capillaries, but not in the blood vasculature. In normal skin and kidney, podoplanin colocalized with vascular endothelial growth factor receptor-3, the only other lymphatic marker presently available. Complementary immunostaining of blood vessels was obtained with established endothelial markers (CD31, CD34, factor VIII-related antigen, and Ulex europaeus I lectin) as well as podocalyxin, another podocytic protein that is also localized in endothelia of blood vessels. Podoplanin specifically immunolabeled endothelia of benign tumorous lesions of undisputed lymphatic origin (lymphangiomas, hygromas) and was detected there as a 38-kd protein by immunoblotting. As paradigms of malignant vascular tumors, poorly differentiated (G3) common angiosarcomas (n = 8), epitheloid angiosarcomas (n = 3), and intestinal Kaposi's sarcomas (n = 5) were examined for their podoplanin content in relation to conventional endothelial markers. The relative number of tumor cells expressing podoplanin was estimated and, although the number of cases in this preliminary study was limited to 16, an apparent spectrum of podoplanin expression emerged that can be divided into a low-expression group in which 0–10% of tumor cells contained podoplanin, a moderate-expression group with 30–60% and a high-expression group with 70–100%. Ten of eleven angiosarcomas and all Kaposi's sarcomas showed mixed expression of both lymphatic and blood vascular endothelial phenotypes. By double labeling, most podoplanin-positive tumor cells coexpressed endothelial markers of blood vessels, whereas few tumor cells were positive for individual markers only. From these results we conclude that (1) podoplanin is a selective marker of lymphatic endothelium; (2) G3 angiosarcomas display a quantitative spectrum of podoplanin-expressing tumor cells; (3) in most angiosarcomas, a varying subset of tumor cells coexpresses podoplanin and endothelial markers of blood vessels; and (4) all endothelial cells of Kaposi's sarcomas expressed the lymphatic marker podoplanin.




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S. Podgrabinska, P. Braun, P. Velasco, B. Kloos, M. S. Pepper, D. G. Jackson, and M. Skobe
Molecular characterization of lymphatic endothelial cells
PNAS, December 10, 2002; 99(25): 16069 - 16074.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. Clarijs, L. Schalkwijk, U. B. Hofmann, D. J. Ruiter, and R. M. W. de Waal
Induction of Vascular Endothelial Growth Factor Receptor-3 Expression on Tumor Microvasculature as a New Progression Marker in Human Cutaneous Melanoma
Cancer Res., December 1, 2002; 62(23): 7059 - 7065.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. E. Akerman, W. C. W. Chan, P. Laakkonen, S. N. Bhatia, and E. Ruoslahti
Nanocrystal targeting in vivo
PNAS, October 1, 2002; 99(20): 12617 - 12621.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
S. F. Schoppmann, P. Birner, J. Stockl, R. Kalt, R. Ullrich, C. Caucig, E. Kriehuber, K. Nagy, K. Alitalo, and D. Kerjaschki
Tumor-Associated Macrophages Express Lymphatic Endothelial Growth Factors and Are Related to Peritumoral Lymphangiogenesis
Am. J. Pathol., September 1, 2002; 161(3): 947 - 956.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
C. Cursiefen, U. Schlotzer-Schrehardt, M. Kuchle, L. Sorokin, S. Breiteneder-Geleff, K. Alitalo, and D. Jackson
Lymphatic Vessels in Vascularized Human Corneas: Immunohistochemical Investigation Using LYVE-1 and Podoplanin
Invest. Ophthalmol. Vis. Sci., July 1, 2002; 43(7): 2127 - 2135.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
S. A. STACKER, M. E. BALDWIN, and M. G. ACHEN
The role of tumor lymphangiogenesis in metastatic spread
FASEB J, July 1, 2002; 16(9): 922 - 934.
[Abstract] [Full Text] [PDF]

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 Physiol. Rev.Home page
L. Jussila and K. Alitalo
Vascular Growth Factors and Lymphangiogenesis
Physiol Rev, July 1, 2002; 82(3): 673 - 700.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
H. Kubo, R. Cao, E. Brakenhielm, T. Makinen, Y. Cao, and K. Alitalo
Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea
PNAS, June 25, 2002; 99(13): 8868 - 8873.
[Abstract] [Full Text] [PDF]

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 Genes Dev.Home page
G. Oliver and M. Detmar
The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature
Genes & Dev., April 1, 2002; 16(7): 773 - 783.
[Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
R. K. Jain and B. T. Fenton
Intratumoral Lymphatic Vessels: A Case of Mistaken Identity or Malfunction?
J Natl Cancer Inst, March 20, 2002; 94(6): 417 - 421.
[Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
D.-H. Kang, J. Kanellis, C. Hugo, L. Truong, S. Anderson, D. Kerjaschki, G. F. Schreiner, and R. J. Johnson
Role of the Microvascular Endothelium in Progressive Renal Disease
J. Am. Soc. Nephrol., March 1, 2002; 13(3): 806 - 816.
[Abstract] [Full Text] [PDF]

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 Cold Spring Harb Symp Quant BiolHome page
T. MAKINEN and K. ALITALO
Molecular Mechanisms of Lymphangiogenesis
Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 189 - 196.
[Abstract] [PDF]

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 JEMHome page
H. Irjala, E.-L. Johansson, R. Grenman, K. Alanen, M. Salmi, and S. Jalkanen
Mannose Receptor Is a Novel Ligand for L-Selectin and Mediates Lymphocyte Binding to Lymphatic Endothelium
J. Exp. Med., October 8, 2001; 194(8): 1033 - 1042.
[Abstract] [Full Text] [PDF]

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 JEMHome page
E. Kriehuber, S. Breiteneder-Geleff, M. Groeger, A. Soleiman, S. F. Schoppmann, G. Stingl, D. Kerjaschki, and D. Maurer
Isolation and Characterization of Dermal Lymphatic and Blood Endothelial Cells Reveal Stable and Functionally Specialized Cell Lineages
J. Exp. Med., September 17, 2001; 194(6): 797 - 808.
[Abstract] [Full Text] [PDF]

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 JEMHome page
T. Karpanen and K. Alitalo
Lymphatic Vessels as Targets of Tumor Therapy?
J. Exp. Med., September 17, 2001; 194(6): F37 - F42.
[Full Text] [PDF]

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 IOVSHome page
R. Clarijs, L. Schalkwijk, D. J. Ruiter, and R. M. W. de Waal
Lack of Lymphangiogenesis Despite Coexpression of VEGF-C and Its Receptor Flt-4 in Uveal Melanoma
Invest. Ophthalmol. Vis. Sci., June 1, 2001; 42(7): 1422 - 1428.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
M. S. Pepper
Lymphangiogenesis and Tumor Metastasis: Myth or Reality?
Clin. Cancer Res., March 1, 2001; 7(3): 462 - 468.
[Abstract] [Full Text]

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 Am. J. Pathol.Home page
R. J. B. Nibbs, E. Kriehuber, P. D. Ponath, D. Parent, S. Qin, J. D. M. Campbell, A. Henderson, D. Kerjaschki, D. Maurer, G. J. Graham, et al.
The {beta}-Chemokine Receptor D6 Is Expressed by Lymphatic Endothelium and a Subset of Vascular Tumors
Am. J. Pathol., March 1, 2001; 158(3): 867 - 877.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
P. Birner, A. Obermair, M. Schindl, H. Kowalski, G. Breitenecker, and G. Oberhuber
Selective Immunohistochemical Staining of Blood and Lymphatic Vessels Reveals Independent Prognostic Influence of Blood and Lymphatic Vessel Invasion in Early-Stage Cervical Cancer
Clin. Cancer Res., January 1, 2001; 7(1): 93 - 97.
[Abstract] [Full Text]

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 Arch SurgHome page
S. D. Nathanson, R. J. Zarbo, D. L. Wachna, C. A. Spence, T. A. Andrzejewski, and J. Abrams
Microvessels That Predict Axillary Lymph Node Metastases in Patients With Breast Cancer
Arch Surg, May 1, 2000; 135(5): 586 - 594.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
H. M. REGELE, E. FILLIPOVIC, B. LANGER, H. POCZEWKI, I. KRAXBERGER, R. E. BITTNER, and D. KERJASCHKI
Glomerular Expression of Dystroglycans Is Reduced in Minimal Change Nephrosis But Not in Focal Segmental Glomerulosclerosis
J. Am. Soc. Nephrol., March 1, 2000; 11(3): 403 - 412.
[Abstract] [Full Text] [PDF]


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