Bone morphogenetic protein-9 inhibits lymphatic vessel formation via activin receptor-like kinase 1 during development and cancer progression

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 47, 2013, Pages 18940-18945

  Yoshimatsu, Yasuhiro ^a   Lee, Yulia G ^b   Akatsu, Yuichi ^a   Taguchi, Luna ^a   Suzuki, Hiroshi I ^a   Cunha, Sara I ^c   Maruyama, Kazuichi ^d   Suzuki, Yuka ^a   Yamazaki, Tomoko ^a   Katsura, Akihiro ^a   Oh, S Paul ^e   Zimmers, Teresa A ^f   Lee, Se Jin ^g   Pietras, Kristian ^c,h   Koh, Gou Young ^b   Miyazono, Kohei ^a   Watabe, Tetsuro ^a,i,j  

^a UNIVERSITY OF TOKYO   (Japan)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c KAROLINSKA INSTITUTE   (Sweden)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^f THOMAS JEFFERSON UNIVERSITY   (United States)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h LUND UNIVERSITY   (Sweden)

ⁱ JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^j TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

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Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; ANGIOPOIETIN RECEPTOR; BONE MORPHOGENETIC PROTEIN 9; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PROX1; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST CARCINOMA; CANCER GROWTH; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; FEMALE; GENE MUTATION; GENE SILENCING; HOMEOBOX; LYMPHANGIOGENESIS; LYMPHOCYTE; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANGIOGENESIS; BLOOD VASCULAR ENDOTHELIAL CELLS; LYMPHANGIOGENESIS;

ACTIVIN RECEPTORS, TYPE II; ANALYSIS OF VARIANCE; ANIMALS; DIAPHRAGM; DNA PRIMERS; GENE EXPRESSION PROFILING; GROWTH DIFFERENTIATION FACTOR 2; HEK293 CELLS; HISTOLOGICAL TECHNIQUES; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LYMPHATIC VESSELS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PERITONITIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84888084861     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1310479110     Document Type: Article

References (34)

1. Karpanen T, Alitalo K (2008) Molecular biology and pathology of lymphangiogenesis. Annu Rev Pathol 3:367-397.
2. Oliver G, Srinivasan RS (2010) Endothelial cell plasticity: How to become and remain a lymphatic endothelial cell. Development 137(3-363-372.
3. Karkkainen MJ, et al. (2004) Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 5(1-74-80.
4. Wigle JT, et al. (2002) An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 21(7-1505-1513.
5. Petrova TV, et al. (2002) Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J 21(17-4593-4599.
6. Mishima K, et al. (2007) Prox1 induces lymphatic endothelial differentiation via integrin alpha9 and other signaling cascades. Mol Biol Cell 18(4-1421-1429.
7. Johnson NC, et al. (2008) Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev 22(23-3282-3291.
8. Maruyama K, et al. (2005) Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest 115(9-2363-2372.
9. He Y, et al. (2004) Preexisting lymphatic endothelium but not endothelial progenitor cells are essential for tumor lymphangiogenesis and lymphatic metastasis. Cancer Res 64(11-3737-3740.
10. Tammela T, Alitalo K (2010) Lymphangiogenesis: Molecular mechanisms and future promise. Cell 140(4-460-476.
11. Kataru RP, et al. (2011) T lymphocytes negatively regulate lymph node lymphatic vessel formation. Immunity 34(1-96-107.
12. Oka M, et al. (2008) Inhibition of endogenous TGF-beta signaling enhances lymphangiogenesis. Blood 111(9-4571-4579.
13. Derynck R, Miyazono K (2008) TGF-β and the TGF-β family, Cold Spring Harbor Monograph Series, eds Derynck R, Miyazono K (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY).
14. Miyazono K, Kamiya Y, Morikawa M (2010) Bone morphogenetic protein receptors and signal transduction. J Biochem 147(1-35-51.
15. McAllister KA, et al. (1994) Endoglin, a TGF-β binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 8(4-345-351.
16. Johnson DW, et al. (1996) Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat Genet 13(2-189-195.
17. Gallione CJ, et al. (2004) A combined syndrome of juvenile polyposis and hereditary haemorrhagic telangiectasia associated with mutations in MADH4 (SMAD4). Lancet 363(9412-852-859.
18. Srinivasan S, et al. (2003) A mouse model for hereditary hemorrhagic telangiectasia (HHT) type 2. Hum Mol Genet 12(5-473-482.
19. Park SO, et al. (2008) ALK5- and TGFBR2-independent role of ALK1 in the pathogenesis of hereditary hemorrhagic telangiectasia type 2. Blood 111(2-633-642.
20. Park SO, et al. (2009) Real-time imaging of de novo arteriovenous malformation in a mouse model of hereditary hemorrhagic telangiectasia. J Clin Invest 119(11-3487-3496.
21. David L, et al. (2008) Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ Res 102(8-914-922.
22. Scharpfenecker M, et al. (2007) BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J Cell Sci 120(Pt 6-964-972.
23. Larrivée B, et al. (2012) ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev Cell 22(3-489-500.
24. Cunha SI, et al. (2010) Genetic and pharmacological targeting of activin receptor-like kinase 1 impairs tumor growth and angiogenesis. J Exp Med 207(1-85-100.
25. Suzuki Y, et al. (2010) BMP-9 induces proliferation of multiple types of endothelial cells in vitro and in vivo. J Cell Sci 123(Pt 10-1684-1692.
26. Niessen K, Zhang G, Ridgway JB, Chen H, Yan M (2010) ALK1 signaling regulates early postnatal lymphatic vessel development. Blood 115(8-1654-1661.
27. Pashmforoush M, et al. (2004) Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block. Cell 117(3-373-386.
28. Brown MA, et al. (2005) Crystal structure of BMP-9 and functional interactions with pro-region and receptors. J Biol Chem 280(26-25111-25118.
29. Ricard N, et al. (2012) BMP9 and BMP10 are critical for postnatal retinal vascular remodeling. Blood 119(25-6162-6171.
30. Yoshimatsu Y, et al. (2011) Ets family members induce lymphangiogenesis through physical and functional interaction with Prox1. J Cell Sci 124(Pt 16-2753-2762.
31. Simirskii VN, Wang Y, Duncan MK (2007) Conditional deletion of β1-integrin from the developing lens leads to loss of the lens epithelial phenotype. Dev Biol 306(2-658-668.
32. Herrera B, van Dinther M, Ten Dijke P, Inman GJ (2009) Autocrine bone morphogenetic protein-9 signals through activin receptor-like kinase-2/Smad1/Smad4 to promote ovarian cancer cell proliferation. Cancer Res 69(24-9254-9262.
33. Ye L, Kynaston H, Jiang WG (2008) Bone morphogenetic protein-9 induces apoptosis in prostate cancer cells, the role of prostate apoptosis response-4. Mol Cancer Res 6(10-1594-1606.
34. Cunha SI, Pietras K (2011) ALK1 as an emerging target for antiangiogenic therapy of cancer. Blood 117(26-6999-7006.