The effect of podoplanin inhibition on lymphangiogenesis under pathological conditions

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 8, 2014, Pages 4813-4822

  Maruyama, Yuko ^a   Maruyama, Kazuichi ^b   Kato, Yukinari ^b   Kajiya, Kentaro ^c   Moritoh, Satoru ^b   Yamamoto, Kotaro ^b   Matsumoto, Yuko ^c   Sawane, Mika ^c   Kerjaschki, Dontscho ^d   Nakazawa, Toru ^b   Kinoshita, Shigeru ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c SHISEIDO RESEARCH CENTER   (Japan)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Lymphangiogenesis; Macrophage; Podoplanin

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NUCLEAR FACTOR; PODOPLANIN; PODOPLANIN ANTIBODY; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORNEA; CORNEA TRANSPLANTATION; EAR; ENZYME LINKED IMMUNOSORBENT ASSAY; GRAFT REJECTION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LYMPH VESSEL; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; MACROPHAGE FUNCTION; MACROPHAGE INFILTRATION; MALE; MOUSE; NONHUMAN; OPHTHALMIC SUTURE; PERITONEAL EXUDATE CELL; PHOSPHORYLATION; PRIORITY JOURNAL; SKIN BIOPSY; SKINFOLD THICKNESS; WESTERN BLOTTING; WOUND HEALING;

LYMPHANGIOGENESIS; MACROPHAGE; PODOPLANIN;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CORNEA; CORNEAL NEOVASCULARIZATION; CORNEAL TRANSPLANTATION; DISEASE MODELS, ANIMAL; ENDOTHELIUM, LYMPHATIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; LYMPHANGIOGENESIS; MACROPHAGES; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; TUMOR NECROSIS FACTOR-ALPHA; WOUND HEALING;

EID: 84905259793     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13711     Document Type: Article

References (37)

1. 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: 385-394.
2. Yuan P, Temam S, El-Naggar A, et al. Overexpression of podoplanin in oral cancer and its association with poor clinical outcome. Cancer. 2006; 107: 563-569.
3. Tong L, Yuan S, Feng F, Zhang H. Role of podoplanin expression in esophageal squamous cell carcinoma: a retrospective study. Dis Esophagus. 2012; 25: 72-80.
4. Mishima K, Kato Y, Kaneko MK, Nishikawa R, Hirose T, Matsutani M. Increased expression of podoplanin in malignant astrocytic tumors as a novel molecular marker of malignant progression. Acta Neuropathol. 2006; 111: 483-488.
5. Martin-Villar E, Scholl FG, Gamallo C, et al. Characterization of human PA2. 26 antigen (T1alpha-2, podoplanin), a small membrane mucin induced in oral squamous cell carcinomas. Int J Cancer. 2005; 113: 899-910.
6. Kato Y, Kaneko M, Sata M, Fujita N, Tsuruo T, Osawa M. Enhanced expression of Aggrus (T1alpha/podoplanin), a platelet-aggregation-inducing factor in lung squamous cell carcinoma. Tumour Biol. 2005; 26: 195-200.
7. Dumoff KL, Chu C, Xu X, Pasha T, Zhang PJ, Acs G. Low D2-40 immunoreactivity correlates with lymphatic invasion and nodal metastasis in early-stage squamous cell carcinoma of the uterine cervix. Mod Pathol. 2005; 18: 97-104.
8. Kato Y, Kaneko MK, Kuno A, et al. Inhibition of tumor cellinduced platelet aggregation using a novel anti-podoplanin antibody reacting with its platelet-aggregation-stimulating domain. Biochem Biophys Res Commun. 2006; 349: 1301-1307.
9. Kawase A, Ishii G, Nagai K, et al. Podoplanin expression by cancer associated fibroblasts predicts poor prognosis of lung adenocarcinoma. Int J Cancer. 2008; 123: 1053-1059.
10. Kunita A, Kashima TG, Morishita Y, et al. The platelet aggregation-inducing factor aggrus/podoplanin promotes pulmonary metastasis. Am J Pathol. 2007; 170: 1337-1347.
11. Renyi-Vamos F, Tovari J, Fillinger J, et al. Lymphangiogenesis correlates with lymph node metastasis, prognosis, and angiogenic phenotype in human non-small cell lung cancer. Clin Cancer Res. 2005; 11: 7344-7353.
12. Nakazawa Y, Takagi S, Sato S, et al. Prevention of hematogenous metastasis by neutralizing mice and its chimeric anti-Aggrus/podoplanin antibodies. Cancer Sci. 2011; 102: 2051-2057.
13. Kato Y, Vaidyanathan G, Kaneko MK, et al. Evaluation of antipodoplanin rat monoclonal antibody NZ-1 for targeting malignant gliomas. Nucl Med Biol. 2010; 37: 785-794.
14. Kaneko MK, Kunita A, Abe S, et al. Chimeric anti-podoplanin antibody suppresses tumor metastasis through neutralization and antibody-dependent cellular cytotoxicity. Cancer Sci. 2012; 103: 1913-1919.
15. Chandramohan V, Bao XH, Kaneko MK, et al. Recombinant anti-podoplanin (NZ-1) immunotoxin for the treatment of malignant brain tumors. Int J Cancer. 2013; 132: 2339-2348.
16. Bertozzi CC, Hess PR, Kahn ML. Platelets: covert regulators of lymphatic development. Arterioscler Thromb Vasc Biol. 2010; 30: 2368-2371.
17. Uhrin P, Zaujec J, Breuss JM, et al. Novel function for blood platelets and podoplanin in developmental separation of blood and lymphatic circulation. Blood. 2010; 115: 3997-4005.
18. Schacht V, Ramirez MI, Hong YK, et al. T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J. 2003; 22: 3546-3556.
19. Mourao-Sa D, Robinson MJ, Zelenay S, et al. CLEC-2 signaling via Syk in myeloid cells can regulate inflammatory responses. Eur J Immunol. 2011; 41: 3040-3053.
20. Kerrigan AM, Navarro-Nunez L, Pyz E, et al. Podoplaninexpressing inflammatory macrophages activate murine platelets via CLEC-2. J Thromb Haemost. 2011; 10: 484-486.
21. Maruyama K, Ii M, Cursiefen C, et al. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest. 2005; 115: 2363-2372.
22. Maruyama K, Nakazawa T, Cursiefen C, et al. The maintenance of lymphatic vessels in the cornea is dependent on the presence of macrophages. Invest Ophthalmol Vis Sci. 2012; 53: 3145-3153.
23. Cursiefen C, Chen L, Borges LP, et al. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest. 2004; 113: 1040-1050.
24. Nakao S, Kuwano T, Tsutsumi-Miyahara C, et al. Infiltration of COX-2-expressing macrophages is a prerequisite for IL-1 betainduced neovascularization and tumor growth. J Clin Invest. 2005; 115: 2979-2991.
25. Kaji C, Tsujimoto Y, Kato Kaneko M, Kato Y, Sawa Y. immunohistochemical examination of novel rat monoclonal antibodies against mouse and human podoplanin. Acta Histochem Cytochem. 2012; 45: 227-237.
26. Kajiya K, Hirakawa S, Detmar M. Vascular endothelial growth factor-A mediates ultraviolet B-induced impairment of lymphatic vessel function. Am J Pathol. 2006; 169: 1496-1503.
27. Kezuka T, Streilein JW. In vitro generation of regulatory CD8{thorn} T cells similar to those found in mice with anterior chamberassociated immune deviation. Invest Ophthalmol Vis Sci. 2000; 41: 1803-1811.
28. Sawane M, Kidoya H, Muramatsu F, Takakura N, Kajiya K. Apelin attenuates UVB-induced edema and inflammation by promoting vessel function. Am J Pathol. 2011; 179: 2691-2697.
29. Zheng Y, Lin H, Ling S. Clinicopathological correlation analysis of (lymph) angiogenesis and corneal graft rejection. Mol Vis. 2011; 17: 1694-1700.
30. Cursiefen C, Chen L, Dana MR, Streilein JW. Corneal lymphangiogenesis: evidence, mechanisms, and implications for corneal transplant immunology. Cornea. 2003; 22: 273-281.
31. Cursiefen C, Cao J, Chen L, et al. Inhibition of hemangiogenesis and lymphangiogenesis after normal-risk corneal transplantation by neutralizing VEGF promotes graft survival. Invest Ophthalmol Vis Sci. 2004; 45: 2666-2673.
32. 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: 575-586.
33. 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.
34. Maruyama K, Asai J, Ii M, Thorne T, Losordo DW, D'Amore PA. Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing. Am J Pathol. 2007; 170: 1178-1191.
35. Yamagami S, Dana MR. The critical role of lymph nodes in corneal alloimmunization and graft rejection. Invest Ophthalmol Vis Sci. 2001; 42: 1293-1298.
36. Cursiefen C, Cao J, Chen L, et al. Inhibition of hemangiogenesis and lymphangiogenesis after normal-risk corneal transplantation by neutralizing VEGF promotes graft survival. Invest Ophthalmol Vis Sci. 2004; 45: 2666-2673.
37. Schorey JS, Cooper AM. Macrophage signalling upon mycobacterial infection: the MAP kinases lead the way. Cell Microbiol. 2003; 5: 133-142.