Podoplanin-Fc reduces lymphatic vessel formation in vitro and in vivo and causes disseminated intravascular coagulation when transgenically expressed in the skin

Blood

Volumn 116, Issue 20, 2010, Pages 4376-4384

  Cueni, Leah N ^a   Chen, Lu ^b   Zhang, Hui ^b   Marino, Daniela ^a   Huggenberger, Reto ^a   Alitalo, Annamari ^a   Bianchi, Roberta ^a   Detmar, Michael ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PODOPLANIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DISSEMINATED INTRAVASCULAR CLOTTING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBOCYTOPENIA;

EID: 78549282833     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-04-278564     Document Type: Article

References (47)

1. Karpanen T, Egeblad M, Karkkainen MJ, et al. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res. 2001;61(5):1786-1790. (Pubitemid 32691984)
2. Kriehuber E, Breiteneder-Geleff S, Groeger M, et al. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med. 2001;194(6):797-808. (Pubitemid 32983015)
3. Petrova TV, Makinen T, Makela TP, et al. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 2002;21(17):4593-4599.
4. Hirakawa S, Hong YK, Harvey N, et al. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am J Pathol. 2003; 162(2):575-586.
5. Wetterwald A, Hoffstetter W, Cecchini MG, et al. Characterization and cloning of the E11 antigen, a marker expressed by rat osteoblasts and osteocytes. Bone. 1996;18(2):125-132. (Pubitemid 26092592)
6. Breiteneder-Geleff S, Soleiman A, Kowalski H, et al. Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. Am J Pathol. 1999;154(2):385-394.
7. Schacht V, Ramirez MI, Hong YK, et al. T1alpha/ podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J. 2003;22(14):3546-3556.
8. Martin-Villar E, Megias D, Castel S, Yurrita MM, Vilaro S, Quintanilla M. Podoplanin binds ERM proteins to activate RhoA and promote epithelial- mesenchymal transition. J Cell Sci. 2006; 119(Pt 21):4541-4553. (Pubitemid 44830653)
9. Cueni LN, Detmar M. Galectin-8 interacts with podoplanin and modulates lymphatic endothelial cell functions. Exp Cell Res. 2009;135:1715-1723.
10. Suzuki-Inoue K, Kato Y, Inoue O, et al. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem. 2007;282(36): 25993-26001.
11. Kato Y, Kaneko MK, Kunita A, et al. Molecular analysis of the pathophysiological binding of the platelet aggregation-inducing factor podoplanin to the C-type lectin-like receptor CLEC-2. Cancer Sci. 2008;99(1):54-61.
12. Kerjaschki D, Regele HM, Moosberger I, et al. Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates. J Am Soc Nephrol. 2004;15(3):603-612. (Pubitemid 38294790)
13. Cueni LN, Detmar M. The lymphatic system in health and disease. Lymphat Res Biol. 2008: 6(3-4):109-122.
14. Banziger-Tobler NE, Halin C, Kajiya K, Detmar M. Growth hormone promotes lymphangiogenesis. Am J Pathol. 2008;173(2):586-597.
15. Shin JW, Huggenberger R, Detmar M. Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial- specific molecule-1 as a novel mediator of lymphangiogenesis. Blood. 2008;112(6): 2318-2326.
16. Streit M, Velasco P, Brown LF, et al. Overexpression of thrombospondin-1 decreases angiogenesis and inhibits the growth of human cutaneous squamous cell carcinomas. Am J Pathol. 1999; 155(2):441-452.
17. Liersch R, Nay F, Lu L, Detmar M. Induction of lymphatic endothelial cell differentiation in embryoid bodies. Blood. 2006;107(3):1214-1216.
18. Chen L, Hamrah P, Cursiefen C, et al. Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity. Nat Med. 2004; 10(8):813-815. (Pubitemid 39070853)
19. Chen L, Cursiefen C, Barabino S, Zhang Q, Dana MR. Novel expression and characterization of lymphatic vessel endothelial hyaluronate receptor 1 (LYVE-1) by conjunctival cells. Invest Ophthalmol Vis Sci. 2005;46(12):4536-4540.
20. Chen L, Huq S, Gardner H, de Fougerolles AR, Barabino S, Dana MR. Very late antigen 1 blockade markedly promotes survival of corneal allografts. Arch Ophthalmol. 2007;125(6):783-788.
21. Albuquerque RJ, Hayashi T, Cho WG, et al. Alternatively spliced vascular endothelial growth factor receptor-2 is an essential endogenous inhibitor of lymphatic vessel growth. Nat Med. 2009;15(9): 1023-1030.
22. Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, Detmar M. Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol. 2005;166(3):913-921. (Pubitemid 40315647)
23. Vassar R, Rosenberg M, Ross S, Tyner A, Fuchs E. Tissue-specific and differentiation-specific expression of a human K14 keratin gene in transgenic mice. Proc Natl Acad Sci U S A. 1989;86(5):1563-1567. (Pubitemid 19078943)
24. Bertozzi CC, Schmaier AA, Mericko P, et al. Platelets regulate lymphatic vascular development through CLEC-2-SLP-76 signaling. Blood. 2010;116(4):661-670.
25. Patnaik SK, Stanley P. Lectin-resistant CHO glycosylation mutants. Methods Enzymol. 2006; 416:159-182.
26. Kaneko M, Kato Y, Kunita A, Fujita N, Tsuruo T, Osawa M. Functional sialylated O-glycan to platelet aggregation on Aggrus (T1alpha/Podoplanin) molecules expressed in Chinese hamster ovary cells. J Biol Chem. 2004;279(37):38838-38843.
27. Kingsley DM, Kozarsky KF, Hobbie L, Krieger M. Reversible defects in O-linked glycosylation and LDL receptor expression in a UDP-Gal/UDP-GalNAc 4-epimerase deficient mutant. Cell. 1986; 44(5):749-759.
28. Cursiefen C, Maruyama K, Jackson DG, Streilein JW, Kruse FE. Time course of angiogenesis and lymphangiogenesis after brief corneal inflammation. Cornea. 2006;25(4):443-447. (Pubitemid 44620130)
29. Zimmer G, Oeffner F, Von Messling V, et al. Cloning and characterization of gp36, a human mucintype glycoprotein preferentially expressed in vascular endothelium. Biochem J. 1999;341(Pt 2): 277-284.
30. Scholl FG, Gamallo C, Vilar S, Quintanilla M. 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. 1999; 112(Pt 24):4601-4613.
31. Kato Y, Fujita N, Kunita A, et al. Molecular identification of Aggrus/T1alpha as a platelet aggregation-inducing factor expressed in colorectal tumors. J Biol Chem. 2003;278(51):51599-51605. (Pubitemid 38020404)
32. Ettinger R, Browning JL, Michie SA, van Ewijk W, McDevitt HO. Disrupted splenic architecture, but normal lymph node development in mice expressing a soluble lymphotoxin-beta receptor-IgG1 fusion protein. Proc Natl Acad Sci U S A. 1996;93(23):13102-13107.
33. Karpanen T, Wirzenius M, Makinen T, et al. Lymphangiogenic growth factor responsiveness is modulated by postnatal lymphatic vessel maturation. Am J Pathol. 2006;169(2):708-718.
34. Luthje K, Cramer SO, Ehrlich S, et al. Transgenic expression of a CD83-immunoglobulin fusion protein impairs the development of immunecompetent CD4-positive T cells. Eur J Immunol. 2006;36(8):2035-2045. (Pubitemid 44251750)
35. Makinen T, Jussila L, Veikkola T, et al. Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat Med. 2001;7(2):199-205.
36. Purpura KA, George SH, Dang SM, Choi K, Nagy A, Zandstra PW. Soluble Flt-1 regulates Flk-1 activation to control hematopoietic and endothelial development in an oxygen-responsive manner. Stem Cells. 2008;26(11):2832-2842.
37. Senn KA, McCoy KD, Maloy KJ, et al. T1-deficient and T1-Fc-transgenic mice develop a normal protective Th2-type immune response following infection with Nippostrongylus brasiliensis. Eur J Immunol. 2000;30(7):1929-1938.
38. 1 provides a marked resistance against pseudorabies virus infection to transgenic mice. Microbiol Immunol. 2009;53(1):8-15.
39. Yoshinaga SK, Whoriskey JS, Khare SD, et al. T-cell co-stimulation through B7RP-1 and ICOS. Nature. 1999;402(6763):827-832.
40. Suzuki-Inoue K, Fuller GL, Garcia A, et al. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood. 2006;107(2):542-549. (Pubitemid 43076377)
41. Abtahian F, Guerriero A, Sebzda E, et al. Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science. 2003;299(5604):247-251.
42. Fu J, Gerhardt H, McDaniel JM, et al. Endothelial cell O-glycan deficiency causes blood/lymphatic misconnections and consequent fatty liver disease in mice. J Clin Invest. 2008;118(11): 3725-3737.
43. Levi M, Ten Cate H. Disseminated intravascular coagulation. N Engl J Med. 1999;341(8):586-592.
44. Kyrle PA, Minar E, Bialonczyk C, Hirschl M, Weltermann A, Eichinger S. The risk of recurrent venous thromboembolism in men and women. N Engl J Med. 2004;350(25):2558-2563.
45. Marenberg ME, Risch N, Berkman LF, Floderus B, de Faire U. Genetic susceptibility to death from coronary heart disease in a study of twins. N Engl J Med. 1994;330(15):1041-1046. (Pubitemid 24106561)
46. McRae S, Tran H, Schulman S, Ginsberg J, Kearon C. Effect of patient's sex on risk of recurrent venous thromboembolism: a meta-analysis. Lancet. 2006;368(9533):371-378.
47. Rothwell PM, Coull AJ, Silver LE, et al. Population- based study of event-rate, incidence, case fatality, and mortality for all acute vascular events in all arterial territories (Oxford Vascular Study). Lancet. 2005;366(9499):1773-1783.