T1α/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema

EMBO Journal

Volumn 22, Issue 14, 2003, Pages 3546-3556

  Schacht, Vivien ^a   Ramirez, Maria I ^b   Hong, Young Kwon ^a   Hirakawa, Satoshi ^a   Feng, Dian ^c   Harvey, Natasha ^d   Williams, Mary ^b   Dvorak, Ann M ^c   Dvorak, Harold F ^c   Oliver, Guillermo ^d   Detmar, Michael ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Angiogenesis; Lymphangiogenesis; Podoplanin; Prox1; T1

Indexed keywords

MEMBRANE PROTEIN; PODOPLANIN; PROTEIN T1 ALPHA; UNCLASSIFIED DRUG; GLYCOPROTEIN; GP38 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; PROSPERO RELATED HOMEOBOX 1 PROTEIN; PROSPERO-RELATED HOMEOBOX 1 PROTEIN; SMALL INTERFERING RNA; T1A 2 PROTEIN, HUMAN; T1A-2 PROTEIN, HUMAN; XLKD1 PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAUSE OF DEATH; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; EPIDERMIS; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; HOMEOBOX; LYMPH VESSEL ENDOTHELIUM; LYMPHEDEMA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROX1 GENE; RESPIRATORY FAILURE; STEM CELL; WILD TYPE; ANIMAL; CELL MOTION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; LYMPHATIC SYSTEM; METABOLISM; MOUSE MUTANT; NEWBORN; PATHOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; ULTRASTRUCTURE; VASCULARIZATION;

ANIMALIA;

ANIMALS; ANIMALS, NEWBORN; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIUM, LYMPHATIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; HOMEODOMAIN PROTEINS; LYMPHATIC SYSTEM; LYMPHEDEMA; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; RNA, SMALL INTERFERING;

EID: 0041312675     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg342     Document Type: Article

References (36)

1. Bartos, V., Kolc, J., Vanecek, R. and Malek, P. (1979) Lymph and blood enzymes and pathologic alterations in canine experimental pancreatitis after administration of benzo-pyrones. Scand. J. Gastroenterol., 14, 343-347.
2. Breiteneder-Geleff, S., Matsui, K., Soleiman, A., Meraner, P., Poczewski, H., Kalt, R., Schaffner, G. and Kerjaschki, D. (1997) Podoplanin, novel 43-kd membrane protein of glomerular epithelial cells, is down-regulated in puromycin nephrosis. Am. J. Pathol., 151, 1141-1152.
3. Carmeliet, P. (2000) Mechanisms of angiogenesis and arteriogenesis. Nat. Med., 6, 389-395.
4. Detmar, M. and Hirakawa, S. (2002) The formation of lymphatic vessels and its importance in the setting of malignancy. J. Exp. Med., 196, 713-718.
5. Dobbs, L.G., Williams, M.C. and Gonzalez, R. (1988) Monoclonal antibodies specific to apical surfaces of rat alveolar type I cells bind to surfaces of cultured, but not freshly isolated, type II cells. Biochim. Biophys Acta, 970, 146-156.
6. Dumont, D.J., Jussila, L., Taipale, J., Lymboussaki, A., Mustonen, T., Pajusola, K., Breitman, M. and Alitalo, K. (1998) Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science, 282, 946-949.
7. Farr, A.G., Berry, M.L., Kim, A., Nelson, A.J., Welch, M.P. and Aruffo, A. (1992) Characterization and cloning of a novel glycoprotein expressed by stromal cells in T-dependent areas of peripheral lymphoid tissues. J. Exp. Med., 176, 1477-1482.
8. Fuchs, E. and Byrne, C. (1994) The epidermis: rising to the surface. Curr. Opin. Genet. Dev., 4, 725-736.
9. Gale, N. et al. (2002) Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning and only the latter role is rescued by angiopoietin-1. Dev. Cell, 3, 411-423.
10. Gandarillas, A., Scholl, F.G., Benito, N., Gamallo, C. and Quintanilla, M. (1997) Induction of PA2.26, a cell-surface antigen expressed by active fibroblasts, in mouse epidermal keratinocytes during carcinogenesis. Mol. Carcinog., 20, 10-18.
11. Gonzalez, R.F. and Dobbs, L.G. (1998) Purification and analysis of RTI40, a type I alveolar epithelial cell apical membrane protein. Biochim. Biophys Acta, 1429, 208-216.
12. Hirakawa, S., Hong, Y.K., Harvey, N., Schacht, V., Matsuda, K., Libermann, T. and Detmar, M. (2003) Transcriptional profiling of isolated human lymphatic versus blood vascular endothelial cells. Am. J. Pathol., 162, 575-586.
13. Hong, Y.K., Harvey, N., Noh, Y.H., Schacht, V., Hirakawa, S., Detmar, M. and Oliver, G. (2002) Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev. Dyn., 225, 351-357.
14. Kriehuber, E., Breiteneder, G.S., Groeger, M., Soleiman, A., Schoppmann, S.F., Stingl, G., Kerjaschki, D. and Maurer, D. (2001) Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J. Exp. Med., 194, 797-808.
15. Maekinen, T. et al. (2001) Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J., 20, 4762-4773.
16. Mallon, E.C. and Ryan, T.J. (1994) Lymphedema and wound healing. Clin. Dermatol., 12, 89-93.
17. Nose, K., Saito, H. and Kuroki, T. (1990) Isolation of a gene sequence induced later by tumor-promoting 12-O-tetradecanoylphorbol-13-acetate in mouse osteoblastic cells (MC3T3-E1) and expressed constitutively in ras-transformed cells. Cell Growth Differ., 1, 511-518.
18. Obeso, J., Weber, J. and Auerbach, R. (1990) A hemangioendothelioma-derived cell line: its use as a model for the study of endothelial cell biology. Lab. Invest., 63, 259-269.
19. Oliver, G. and Detmar, M. (2002) The rediscovery of the lymphatic system. Old and new insights into the development and biological function of lymphatic vascular system. Genes Dev., 16, 773-783.
20. Petrova, T.V. et al. (2002) Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J., 21, 4593-4599.
21. Polonskaja, R. (1935) The connections between the superficial and deep lymphatic vessels of the lower limb. Anat. Anz., 81, 247-256.
22. Prevo, R., Banerji, S., Ferguson, D.J., Clasper, S. and Jackson, D.G. (2001) Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium. J. Biol. Chem., 276, 19420-19430.
23. Ramirez, M.I., Millien, G., Hinds, A., Cao, Y., Seldin, D.C. and Williams, M.C. (2003) T1α, a lung type I cell differentiation gene, is required for normal lung cell proliferation and alveolus formation at birth. Dev. Biol., 256, 61-72.
24. Rishi, A.K., Joyce-Brady, M., Fisher, J., Dobbs, L.G., Floros, J., VanderSpek, J., Brody, J.S. and Williams, M.C. (1995) Cloning, characterization and development expression of a rat lung alveolar type I cell gene in embryonic endodermal and neural derivatives. Dev. Biol., 167, 294-306.
25. Sabin, F.R. (1902) On the origin of the lymphatic system from the veins and the development of the lymph hearts and thoracic duct in the pig. Am. J. Anat., 1, 367-389.
26. Scholl, F.G., Gamallo, C., Vilaro, S. and Quintanilla, M. (1999) Identification of PA2.26 antigen as a novel cell-surface mucin-type glycoprotein that induces plasma membrane extensions and increased motility in keratinocytes. J. Cell Sci., 112, 4601-4613.
27. Skobe, M. and Detmar, M. (2000) Structure, function and molecular control of the skin lymphatic system. J. Investig. Dermatol. Symp. Proc., 5, 14-19.
28. Streit, M., Velasco, P., Brown, L.F., Skobe, M., Richard, L., Riccardi, L., Lawler, J. and Detmar, M. (1999) Overexpression of thrombospondin-1 decreases angiogenesis and inhibits the growth of human cutaneous squamous cell carcinomas. Am. J. Pathol., 155, 441-452.
29. Wetterwald, A., Hoffstetter, W., Cecchini, M.G., Lanske, B., Wagner, C., Fleisch, H. and Atkinson, M. (1996) Characterization and cloning of the E11 antigen, a marker expressed by rat osteoblasts and osteocytes. Bone, 18, 125-132.
30. Wigle, J.T. and Oliver, G. (1999) Prox1 function is required for the development of the murine lymphatic system. Cell, 98, 769-778.
31. Wigle, J.T., Harvey, N., Detmar, M., Lagutina, I., Grosveld, G., Gunn, M.D., Jackson, D.G. and Oliver, G. (2002) An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J., 21, 1505-1513.
32. Williams, M.C. (2003) Alveolar type I cells: molecular phenotype and development. Annu. Rev. Physiol., 65, 669-695.
33. Williams, M.C., Cao, Y., Hinds, A., Rishi, A.K. and Wetterwald, A. (1996) T1 α protein is developmentally regulated and expressed by alveolar type I cells, choroid plexus and ciliary epithelia of adult rats. Am. J. Respir. Cell Mol. Biol., 14, 577-585.
34. Yuan, L., Moyon, D., Pardanaud, L., Breant, C., Karkkainen, M.J., Alitalo, K. and Eichmann, A. (2002) Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development, 129, 4797-4806.
35. Zimmer, G., Lottspeich, F., Maisner, A., Klenk, H.D. and Herrler, G. (1997) Molecular characterization of gp40, a mucin-type glycoprotein from the apical plasma membrane of Madin-Darby canine kidney cells (type I). Biochem. J., 326, 99-108.
36. Zimmer, G., Oeffner, F., Von Messling, V., Tschernig, T., Groness, H.J., Klenk, H.D. and Herrler, G. (1999) Cloning and characterization of gp36, a human mucin-type glycoprotein preferentially expressed in vascular endothelium. Biochem. J., 341, 277-284.