Activation of the epidermal growth factor receptor promotes lymphangiogenesis in the skin

Journal of Dermatological Science

Volumn 71, Issue 3, 2013, Pages 184-194

  Marino, Daniela ^a   Angehrn, Yvonne ^a   Klein, Sarah ^a   Riccardi, Sabrina ^a   Baenziger Tobler, Nadja ^a   Otto, Vivianne I ^a   Pittelkow, Mark ^b   Detmar, Michael ^a  

^a ETH ZURICH   (Switzerland)

^b MAYO CLINIC   (United States)

Author keywords

Angiogenesis; EGF; EGF receptor; Lymphangiogenesis

Indexed keywords

AMPHIREGULIN; BLOCKING ANTIBODY; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; GROWTH FACTOR; LYMPHANGIOGENESIS FACTOR; PROTEIN INHIBITOR; PROTEIN TYROSINE KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FEMALE; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LYMPH VESSEL; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN; TRANSGENIC MOUSE;

ANGIOGENESIS; EGF; EGF RECEPTOR; LYMPHANGIOGENESIS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYOID BODIES; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; EPIDERMAL GROWTH FACTOR; FEMALE; GLYCOPROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHANGIOGENESIS; MICE; MICE, TRANSGENIC; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; SKIN;

EID: 84881555986     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2013.04.024     Document Type: Article

References (41)

1. Cueni L.N., Detmar M. New insights into the molecular control of the lymphatic vascular system and its role in disease. J Invest Dermatol 2006, 126:2167-2177.
2. Breiteneder-Geleff S., Soleiman A., Horvat R., Amann G., Kowalski H., Kerjaschki D. Podoplanin - a specific marker for lymphatic endothelium expressed in angiosarcoma. Verh Dtsch Ges Pathol 1999, 83:270-275.
3. Banerji S., Ni J., Wang S.X., Clasper S., Su J., Tammi R., et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 1999, 144:789-801.
4. Goldman J., Rutkowski J.M., Shields J.D., Pasquier M.C., Cui Y., Schmokel H.G., et al. Cooperative and redundant roles of VEGFR-2 and VEGFR-3 signaling in adult lymphangiogenesis. FASEB J 2007, 21:1003-1012.
5. Veikkola T., Jussila L., Makinen T., Karpanen T., Jeltsch M., Petrova T.V., et al. Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J 2001, 20:1223-1231.
6. Bjorndahl M.A., Cao R., Burton J.B., Brakenhielm E., Religa P., Galter D., et al. Vascular endothelial growth factor-a promotes peritumoral lymphangiogenesis and lymphatic metastasis. Cancer Res 2005, 65:9261-9268.
7. Hirakawa S., Kodama S., Kunstfeld R., Kajiya K., Brown L.F., Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 2005, 201:1089-1099.
8. Hong Y.K., Lange-Asschenfeldt B., Velasco P., Hirakawa S., Kunstfeld R., Brown L.F., et al. VEGF-A promotes tissue repair-associated lymphatic vessel formation via VEGFR-2 and the alpha1beta1 and alpha2beta1 integrins. FASEB J 2004, 18:1111-1113.
9. Cueni L.N., Detmar M. The lymphatic system in health and disease. Lymphat Res Biol 2008, 6:109-122.
10. Liersch R., Nay F., Lu L., Detmar M. Induction of lymphatic endothelial cell differentiation in embryoid bodies. Blood 2006, 107:1214-1216.
11. Marino D., Dabouras V., Brandli A.W., Detmar M. A role for all-trans-retinoic acid in the early steps of lymphatic vasculature development. J Vasc Res 2010, 48:236-251.
12. Kajiya K., Hirakawa S., Ma B., Drinnenberg I., Detmar M. Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J 2005, 24:2885-2895.
13. Detmar M., Tenorio S., Hettmannsperger U., Ruszczak Z., Orfanos C.E. Cytokine regulation of proliferation and ICAM-1 expression of human dermal microvascular endothelial cells in vitro. J Invest Dermatol 1992, 98:147-153.
14. Cook P.W., Piepkorn M., Clegg C.H., Plowman G.D., DeMay J.M., Brown J.R., et al. Transgenic expression of the human amphiregulin gene induces a psoriasis-like phenotype. J Clin Invest 1997, 100:2286-2294.
15. Kalin R.E., Banziger-Tobler N.E., Detmar M., Brandli A.W. An in vivo chemical library screen in Xenopus tadpoles reveals novel pathways involved in angiogenesis and lymphangiogenesis. Blood 2009, 114:1110-1122.
16. Hannig M., Figulla H.R., Sauer H., Wartenberg M. Control of leucocyte differentiation from embryonic stem cells upon vasculogenesis and confrontation with tumour tissue. J Cell Mol Med 2010, 14:303-312.
17. Gebaeck T., Schulz M.M., Koumoutsakos P., Detmar M. TScratch: a novel and simple software tool for automated analysis of monolayer wound healing assays. Biotechniques 2009, 46:265-274.
18. Brignola P.S., Lackey K., Kadwell S.H., Hoffman C., Horne E., Carter H.L., et al. Comparison of the biochemical and kinetic properties of the type 1 receptor tyrosine kinase intracellular domains. Demonstration of differential sensitivity to kinase inhibitors. J Biol Chem 2002, 277:1576-1585.
19. Riese D.J., Stern D.F. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 1998, 20:41-48.
20. Wong R.W. Transgenic and knock-out mice for deciphering the roles of EGFR ligands. Cell Mol Life Sci 2003, 60:113-118.
21. Baker C.H., Kedar D., McCarty M.F., Tsan R., Weber K.L., Bucana C.D., et al. Blockade of epidermal growth factor receptor signaling on tumor cells and tumor-associated endothelial cells for therapy of human carcinomas. Am J Pathol 2002, 161:929-938.
22. Kumar R., Yarmand-Bagheri R. The role of HER2 in angiogenesis. Semin Oncol 2001, 28:27-32.
23. Schreiber A.B., Winkler M.E., Derynck R. Transforming growth factor-alpha: a more potent angiogenic mediator than epidermal growth factor. Science 1986, 232:1250-1253.
24. Detmar M., Brown L.F., Claffey K.P., Yeo K.T., Kocher O., Jackman R.W., et al. Overexpression of vascular permeability factor/vascular endothelial growth factor and its receptors in psoriasis. J Exp Med 1994, 180:1141-1146.
25. Amin D.N., Hida K., Bielenberg D.R., Klagsbrun M. Tumor endothelial cells express epidermal growth factor receptor (EGFR) but not ErbB3 and are responsive to EGF and to EGFR kinase inhibitors. Cancer Res 2006, 66:2173-2180.
26. Sini P., Wyder L., Schnell C., O'Reilly T., Littlewood A., Brandt R., et al. The antitumor and antiangiogenic activity of vascular endothelial growth factor receptor inhibition is potentiated by ErbB1 blockade. Clin Cancer Res 2005, 11:4521-4532.
27. Liu N.F., He Q.L. The regulatory effects of cytokines on lymphatic angiogenesis. Lymphology 1997, 30:3-12.
28. Rebhun R.B., Langley R.R., Yokoi K., Fan D., Gershenwald J.E., Fidler I.J. Targeting receptor tyrosine kinase on lymphatic endothelial cells for the therapy of colon cancer lymph node metastasis. Neoplasia 2006, 8:747-757.
29. Kunstfeld R., Hirakawa S., Hong Y.K., Schacht V., Lange-Asschenfeldt B., Velasco P., et al. Induction of cutaneous delayed-type hypersensitivity reactions in VEGF-A transgenic mice results in chronic skin inflammation associated with persistent lymphatic hyperplasia. Blood 2004, 104:1048-1057.
30. Dvorak H.F., Detmar M., Claffey K.P., Nagy J.A., van de Water L., Senger D.R. Vascular permeability factor/vascular endothelial growth factor: an important mediator of angiogenesis in malignancy and inflammation. Int Arch Allergy Immunol 1995, 107:233-235.
31. Al-Nedawi K., Meehan B., Kerbel R.S., Allison A.C., Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A 2009, 106:3794-3799.
32. Herbst R.S., Sandler A. Bevacizumab and erlotinib: a promising new approach to the treatment of advanced NSCLC. Oncologist 2008, 13:1166-1176.
33. Tsimboukis S., Merikas I., Karapanagiotou E.M., Saif M.W., Syrigos K.N. Erlotinib-induced skin rash in patients with non-small-cell lung cancer: pathogenesis, clinical significance, and management. Clin Lung Cancer 2009, 10:106-111.
34. Petit A.M., Rak J., Hung M.C., Rockwell P., Goldstein N., Fendly B., et al. Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor tyrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am J Pathol 1997, 151:1523-1530.
35. Perrotte P., Matsumoto T., Inoue K., Kuniyasu H., Eve B.Y., Hicklin D.J., et al. Anti-epidermal growth factor receptor antibody C225 inhibits angiogenesis in human transitional cell carcinoma growing orthotopically in nude mice. Clin Cancer Res 1999, 5:257-265.
36. Perez-Soler R., Saltz L. Cutaneous adverse effects with HER1/EGFR-targeted agents: is there a silver lining?. J Clin Oncol 2005, 23:5235-5246.
37. Barbaud A., Granel F., Waton J. Poreaux C: how to manage hypersensitivity reactions to biological agents?. Eur J Dermatol 2011, 21:667-674.
38. Settle S.H., Washington K., Lind C., Itzkowitz S., Fiske W.H., Burdick J.S., et al. Chronic treatment of Menetrier's disease with Erbitux: clinical efficacy and insight into pathophysiology. Clin Gastroenterol Hepatol 2005, 3:654-659.
39. Von Minckwitz G., Jonat W., Fasching P., du Bois A., Kleeberg U., Luck H.J., et al. A multicentre phase II study on gefitinib in taxane- and anthracycline-pretreated metastatic breast cancer. Breast Cancer Res Treat 2005, 89:165-172.
40. Adamczyk K.A., Klein-Scory S., Tehrani M.M., Warnken U., Schmiegel W., Schnolzer M., et al. Characterization of soluble and exosomal forms of the EGFR released from pancreatic cancer cells. Life Sci 2011, 89:304-312.
41. Nilsson I., Bahram F., Li X., Gualandi L., Koch S., Jarvius M., et al. VEGF receptor 2/-3 heterodimers detected in situ by proximity ligation on angiogenic sprouts. EMBO J 2010, 29:1377-1388.