Antagonism and synergy between extracellular bmp modulators tsg and bmper balance blood vessel formation

Journal of Cell Science

Volumn 126, Issue 14, 2013, Pages 3082-3094

  Heinke, Jennifer ^a   Juschkat, Maria ^a   Charlet, Anne ^a   Mnich, Leonie ^a   Helbing, Thomas ^a   Bode, Christoph ^a   Moser, Martin ^a   Patterson, Cam ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; BMP modulators; Endothelial cells; Signalling; Zebrafish

Indexed keywords

CHORDIN; NOGGIN; SMAD PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION; WESTERN BLOTTING; ZEBRA FISH;

ANGIOGENESIS; BMP MODULATORS; ENDOTHELIAL CELLS; SIGNALLING; ZEBRAFISH;

ANIMALS; BLOOD VESSELS; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELL GROWTH PROCESSES; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HOMEOSTASIS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; ONCOGENE PROTEIN V-AKT; PROTEINS; RNA, SMALL INTERFERING; SMAD PROTEINS; ZEBRAFISH;

EID: 84880693575     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.122333     Document Type: Article

References (70)

1. Abreu, J. G., Ketpura, N. I., Reversade, B. and De Robertis, E. M. (2002). Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGFbeta. Nat. Cell Biol. 4, 599-604.
2. Adams, R.H. and Alitalo, K. (2007). Molecularregulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. CellBiol.8,464-478.
3. Ambrosio, A. L., Taelman, V. F., Lee, H. X., Metzinger, C. A., Coffinier, C. and De Robertis, E. M. (2008). Crossveinless-2 Is a BMP feedback inhibitor that binds Chordin/BMP to regulate Xenopus embryonic patterning. Dev. Cell 15, 248-260.
4. Balemans, W. and Van Hul, W. (2002). Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 250, 231-250.
5. Bier, E. (2008). Intriguing extracellular regulation of BMP signaling. Dev. Cell 15, 176-177.
6. Bragdon, B., Moseychuk, O., Saldanha, S., King, D., Julian, J. and Nohe, A. (2011). Bone morphogenetic proteins: a critical review. Cell. Signal. 23, 609-620.
7. Carmeliet, P. and Jain, R. K. (2011). Molecular mechanisms and clinical applications of angiogenesis. Nature 473, 298-307.
8. Chang, C., Holtzman, D. A., Chau, S., Chickering, T., Woolf, E. A., Holmgren, L. M., Bodorova, J., Gearing, D. P., Holmes, W. E. and Brivanlou, A. H. (2001). Twisted gastrulation can function as a BMP antagonist. Nature 410, 483-487.
9. Chiodelli, P., Mitola, S., Ravelli, C., Oreste, P., Rusnati, M. and Presta, M. (2011). Heparan sulfate proteoglycans mediate the angiogenic activity of the vascular endothelial growth factor receptor-2 agonist gremlin. Arterioscler. Thromb. Vasc. Biol. 31, e116-e127.
10. David, L., Feige, J. J. and Bailly, S. (2009). Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev. 20, 203-212.
11. Heinke, J., Wehofsits, L., Zhou, Q., Zoeller, C., Baar, K. M., Helbing, T., Laib, A., Augustin, H., Bode, C., Patterson, C. et al. (2008). BMPER is an endothelial cell regulator and controls bone morphogenetic protein-4-dependent angiogenesis. Circ. Res. 103, 804-812.
12. Heinke, J., Kerber, M., Rahner, S., Mnich, L., Lassmann, S., Helbing, T., Werner, M., Patterson, C., Bode, C. and Moser, M. (2012a). Bone morphogenetic protein modulator BMPER is highly expressed in malignant tumors and controls invasive cell behavior. Oncogene 31, 2919-2930.
13. Heinke, J., Patterson, C. and Moser, M. (2012b). Life is a pattern: vascular assembly within the embryo. Front. Biosci. (Elite Ed.) 4, 2269-2288.
14. Helbing, T., Rothweiler, R., Heinke, J., Goetz, L., Diehl, P., Zirlik, A., Patterson, C., Bode, C. and Moser, M. (2010). BMPER is upregulated by statins and modulates endothelial inflammation by intercellular adhesion molecule-1. Arterioscler. Thromb. Vasc. Biol. 30, 554-560.
15. Helbing, T., Rothweiler, R., Ketterer, E., Goetz, L., Heinke, J., Grundmann, S., Duerschmied, D., Patterson, C., Bode, C. and Moser, M. (2011). BMP activity controlled by BMPER regulates the proinflammatory phenotype of endothelium. Blood 118, 5040-5049.
16. Herbert, S. P. and Stainier, D. Y. (2011). Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat. Rev. Mol. Cell Biol. 12, 551-564.
17. Herrera, B. and Inman, G. J. (2009). A rapid and sensitive bioassay for the simultaneous measurement of multiple bone morphogenetic proteins. Identification and quantification of BMP4, BMP6 and BMP9 in bovine and human serum. BMC Cell Biol. 10, 20.
18. Horowitz, A. and Simons, M. (2008). Branching morphogenesis. Circ. Res. 103, 784-795.
19. Ikeya, M., Nosaka, T., Fukushima, K., Kawada, M., Furuta, Y., Kitamura, T. and Sasai, Y. (2008). Twisted gastrulation mutation suppresses skeletal defect phenotypes in Crossveinless 2 mutant mice. Mech. Dev. 125, 832-842.
20. Ikeya, M., Fukushima, K., Kawada, M., Onishi, S., Furuta, Y., Yonemura, S., Kitamura, T., Nosaka, T. and Sasai, Y. (2010). Cv2, functioning as a pro-BMP factor via twisted gastrulation, is required for early development of nephron precursors. Dev. Biol. 337, 405-414.
21. Kelley, R., Ren, R., Pi, X., Wu, Y., Moreno, I., Willis, M., Moser, M., Ross, M., Podkowa, M., Attisano, L. et al. (2009). A concentration-dependent endocytic trap and sink mechanism converts Bmper from an activator to an inhibitor of Bmp signaling. J. Cell Biol. 184, 597-609.
22. Khoo, C. P., Micklem, K. and Watt, S. M. (2011). A comparison of methods for quantifying angiogenesis in the Matrigel assay in vitro. Tissue Eng. Part C Methods 17, 895-906.
23. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
24. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
25. Lillis, A. P., Van Duyn, L. B., Murphy-Ullrich, J. E. and Strickland, D. K. (2008). LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol. Rev. 88, 887-918.
26. Little, S. C. and Mullins, M. C. (2004). Twisted gastrulation promotes BMP signaling in zebrafish dorsal-ventral axial patterning. Development 131, 5825-5835.
27. Lugus, J. J., Chung, Y. S., Mills, J. C., Kim, S. I., Grass, J., Kyba, M., Doherty, J. M., Bresnick, E. H. and Choi, K. (2007). GATA2 functions at multiple steps in hemangioblast development and differentiation. Development 134, 393-405.
28. Marshall, C. J., Kinnon, C. and Thrasher, A. J. (2000). Polarized expression of bone morphogenetic protein-4 in the human aorta-gonad-mesonephros region. Blood 96, 1591-1593.
29. Martin, P. and Parkhurst, S. M. (2004). Parallels between tissue repair and embryo morphogenesis. Development 131, 3021-3034.
30. Mitola, S., Ravelli, C., Moroni, E., Salvi, V., Leali, D., Ballmer-Hofer, K., Zammataro, L. and Presta, M. (2010). Gremlin is a novel agonist of the major proangiogenic receptor VEGFR2. Blood 116, 3677-3680.
31. Moreno-Miralles, I., Schisler, J. C. and Patterson, C. (2009). New insights into bone morphogenetic protein signaling: focus on angiogenesis. Curr. Opin. Hematol. 16, 195-201.
32. Moreno-Miralles, I., Ren, R., Moser, M., Hartnett, M. E. and Patterson, C. (2011). Bone morphogenetic protein endothelial cell precursor-derived regulator regulates retinal angiogenesis in vivo in a mouse model of oxygen-induced retinopathy. Arterioscler. Thromb. Vasc. Biol. 31, 2216-2222.
33. Moser, M., Binder, O., Wu, Y., Aitsebaomo, J., Ren, R., Bode, C., Bautch, V. L., Conlon, F. L. and Patterson, C. (2003). BMPER, a novel endothelial cell precursorderived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol. Cell. Biol. 23, 5664-5679.
34. Moser, M., Yu, Q., Bode, C., Xiong, J. W. and Patterson, C. (2007). BMPER is a conserved regulator of hematopoietic and vascular development in zebrafish. J. Mol. Cell. Cardiol. 43, 243-253.
35. Moya, I. M., Umans, L., Maas, E., Pereira, P. N., Beets, K., Francis, A., Sents, W., Robertson, E. J., Mummery, C. L., Huylebroeck, D. et al. (2012). Stalk cell phenotype depends on integration of Notch and Smad1/5 signaling cascades. Dev. Cell 22, 501-514.
36. Muñoz-Chápuli, R., Quesada, A. R. and Angel Medina, M. (2004). Angiogenesis and signal transduction in endothelial cells. Cell. Mol. Life Sci. 61, 2224-2243.
37. Muratoglu, S. C., Mikhailenko, I., Newton, C., Migliorini, M. and Strickland, D. K. (2010). Low density lipoprotein receptor-related protein 1 (LRP1) forms a signaling complex with platelet-derived growth factor receptor-beta in endosomes and regulates activation of the MAPK pathway. J. Biol. Chem. 285, 14308-14317.
38. Nimmagadda, S., Geetha Loganathan, P., Huang, R., Scaal, M., Schmidt, C. and Christ, B. (2005). BMP4 and noggin control embryonic blood vessel formation by antagonistic regulation of VEGFR-2 (Quek1) expression. Dev. Biol. 280, 100-110.
39. Nosaka, T., Morita, S., Kitamura, H., Nakajima, H., Shibata, F., Morikawa, Y., Kataoka, Y., Ebihara, Y., Kawashima, T., Itoh, T. et al. (2003). Mammalian twisted gastrulation is essential for skeleto-lymphogenesis. Mol. Cell. Biol. 23, 2969-2980.
40. Oelgeschläger, M., Larraín, J., Geissert, D. and De Robertis, E. M. (2000). The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling. Nature 405, 757-763.
41. Olsson, A. K., Dimberg, A., Kreuger, J. and Claesson-Welsh, L. (2006). VEGF receptor signalling-in control of vascular function. Nat. Rev. Mol. Cell Biol. 7, 359-371.
42. Pi, X., Lockyer, P., Dyer, L. A., Schisler, J. C., Russell, B., Carey, S., Sweet, D. T., Chen, Z., Tzima, E., Willis, M. S. et al. (2012a). Bmper inhibits endothelial expression of inflammatory adhesion molecules and protects against atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 32, 2214-2222.
43. Pi, X., Schmitt, C. E., Xie, L., Portbury, A. L., Wu, Y., Lockyer, P., Dyer, L. A., Moser, M., Bu, G., Flynn, E. J. et al. (2012b). An LRP1-dependent endocytic mechanism governs the signaling output of the bmp system in endothelial cells and in angiogenesis. Circ. Res. 111, 564-574.
44. Piccolo, S., Sasai, Y., Lu, B. and De Robertis, E. M. (1996). Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589-598.
45. Ponce, M. L. (2009). Tube formation: an in vitro matrigel angiogenesis assay. Methods Mol. Biol. 467, 183-188.
46. Potente, M., Gerhardt, H. and Carmeliet, P. (2011). Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887.
47. Reese, D. E., Hall, C. E. and Mikawa, T. (2004). Negative regulation of midline vascular development by the notochord. Dev. Cell 6, 699-708.
48. Risau, W. and Flamme, I. (1995). Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11, 73-91.
49. Ross, J. J., Shimmi, O., Vilmos, P., Petryk, A., Kim, H., Gaudenz, K., Hermanson, S., Ekker, S. C., O'Connor, M. B. and Marsh, J. L. (2001). Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 410, 479-483.
50. Scharpfenecker, M., van Dinther, M., Liu, Z., van Bezooijen, R. L., Zhao, Q., Pukac, L., Löwik, C. W. and ten Dijke, P. (2007). BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J. Cell Sci. 120, 964-972.
51. Schmierer, B. and Hill, C. S. (2007). TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat. Rev. Mol. Cell Biol. 8, 970-982.
52. Schmittgen, T. D. and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108.
53. Scott, I. C., Blitz, I. L., Pappano, W. N., Maas, S. A., Cho, K. W. and Greenspan, D. S. (2001). Homologues of Twisted gastrulation are extracellular cofactors in antagonism of BMP signalling. Nature 410, 475-478.
54. Serpe, M., Umulis, D., Ralston, A., Chen, J., Olson, D. J., Avanesov, A., Othmer, H., O'Connor, M. B. and Blair, S. S. (2008). The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev. Cell 14, 940-953.
55. Shiojima, I. and Walsh, K. (2002). Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 90, 1243-1250.
56. Sieber, C., Kopf, J., Hiepen, C. and Knaus, P. (2009). Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev. 20, 343-355.
57. Smith, W. C. and Harland, R. M. (1992). Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829-840.
58. Sonnemann, K. J. and Bement, W. M. (2011). Wound repair: toward understanding and integration of single-cell and multicellular wound responses. Annu. Rev. Cell Dev. Biol. 27, 237-263.
59. Stabile, H., Mitola, S., Moroni, E., Belleri, M., Nicoli, S., Coltrini, D., Peri, F., Pessi, A., Orsatti, L., Talamo, F. et al. (2007). Bone morphogenic protein antagonist Drm/gremlin is a novel proangiogenic factor. Blood 109, 1834-1840.
60. ten Dijke, P. and Arthur, H. M. (2007). Extracellular control of TGFbeta signalling in vascular development and disease. Nat. Rev. Mol. Cell Biol. 8, 857-869.
61. Umulis, D., O'Connor, M. B. and Blair, S. S. (2009). The extracellular regulation of bone morphogenetic protein signaling. Development 136, 3715-3728.
62. Wagner, D. O., Sieber, C., Bhushan, R., Börgermann, J. H., Graf, D. and Knaus, P. (2010). BMPs: from bone to body morphogenetic proteins. Sci. Signal. 3, mr1.
63. Westerfield, M. (1995). The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio). University of Oregon Press, Eugene.
64. Wiley, D. M., Kim, J. D., Hao, J., Hong, C. C., Bautch, V. L. and Jin, S. W. (2011). Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nat. Cell Biol. 13, 686-692.
65. Wong, M. L. and Medrano, J. F. (2005). Real-time PCR for mRNA quantitation. Biotechniques 39, 75-85.
66. Xie, J. and Fisher, S. (2005). Twisted gastrulation enhances BMP signaling through chordin dependent and independent mechanisms. Development 132, 383-391.
67. Yamamoto, Y. and Oelgeschläger, M. (2004). Regulation of bone morphogenetic proteins in early embryonic development. Naturwissenschaften 91, 519-534.
68. Zakin, L. and De Robertis, E. M. (2004). Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development. Development 131, 413-424.
69. Zakin, L., Metzinger, C. A., Chang, E. Y., Coffinier, C. and De Robertis, E. M. (2008). Development of the vertebral morphogenetic field in the mouse: interactions between Crossveinless-2 and Twisted Gastrulation. Dev. Biol. 323, 6-18.
70. Zhou, Q., Heinke, J., Vargas, A., Winnik, S., Krauss, T., Bode, C., Patterson, C. and Moser, M. (2007). ERK signaling is a central regulator for BMP-4 dependent capillary sprouting. Cardiovasc. Res. 76, 390-399.