Bone Morphogenetic Protein 4 Mediates Apoptosis of Capillary Endothelial Cells during Rat Pupillary Membrane Regression

REFERENCES

• Azmi, T. I., and J. D. O'Shea. 1984. Mechanism of deletion of endothelial cells during regression of the corpus luteum. Lab. Investig. 51: 206–217.
   PubMed Web of Science ®Google Scholar
• Boise, L. H., M. Gonzalez-Garcia, C. E. Postema, L. Ding, T. Lindsten, L. A. Turka, X. Mao, G. Nunez, and C. B. Thompson. 1993. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74: 597–608.
   PubMed Web of Science ®Google Scholar
• Cho, A., D. W. Courtman, and B. L. Langille. 1995. Apoptosis (programmed cell death) in arteries of the neonatal lamb. Circ. Res. 76: 168–175.
   PubMed Web of Science ®Google Scholar
• Cho, K. W., and I. L. Blitz. 1998. BMPs, Smads and metalloproteases: extracellular and intracellular modes of negative regulation. Curr. Opin. Genet. Dev. 8: 443–449.
   PubMedGoogle Scholar
• Coucouvanis, E., and G. R. Martin. 1999. BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126: 535–546.
   PubMed Web of Science ®Google Scholar
• Dick, A., W. Risau, and H. Drexler. 1998. Expression of Smad1 and Smad2 during embryogenesis suggests a role in organ development. Dev. Dyn. 211: 293–305.
   PubMedGoogle Scholar
• Diez-Roux, G., and R. A. Lang. 1997. Macrophages induce apoptosis in normal cells in vivo. Development 124: 3633–3638.
   PubMed Web of Science ®Google Scholar
• Ferrari, D., A. C. Lichtler, Z. Z. Pan, C. N. Dealy, W. B. Upholt, and R. A. Kosher. 1998. Ectopic expression of Msx-2 in posterior limb bud mesoderm impairs limb morphogenesis while inducing BMP-4 expression, inhibiting cell proliferation, and promoting apoptosis. Dev. Biol. 197: 12–24.
   PubMedGoogle Scholar
• Furuta, Y., and B. L. Hogan. 1998. BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12: 3764–3775.
   PubMed Web of Science ®Google Scholar
• Furuta, Y., D. W. Piston, and B. L. Hogan. 1997. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124: 2203–2212.
   PubMed Web of Science ®Google Scholar
• Ganan, Y., D. Macias, M. Duterque-Coquillaud, M. A. Ros, and J. M. Hurle. 1996. Role of TGFβs and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122: 2349–2357.
   PubMed Web of Science ®Google Scholar
• Gobe, G., J. Browning, T. Howard, N. Hogg, C. Winterford, and R. Cross. 1997. Apoptosis occurs in endothelial cells during hypertension-induced microvascular rarefaction. J. Struct. Biol. 118: 63–72.
   PubMed Web of Science ®Google Scholar
• Goede, V., T. Schmidt, S. Kimmina, D. Kozian, and H. G. Augustin. 1998. Analysis of blood vessel maturation processes during cyclic ovarian angiogenesis. Lab. Investig. 78: 1385–1394.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Garcia, M., R. Perez-Ballestero, L. Ding, L. Duan, L. H. Boise, C. B. Thompson, and G. Nunez. 1994. bcl-XL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development 120: 3033–3042.
   PubMedGoogle Scholar
• Graham, A., P. Francis-West, P. Brickell, and A. Lumsden. 1994. The signalling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature 372: 684–686.
   PubMed Web of Science ®Google Scholar
• Gross, R. E., M. F. Mehler, P. C. Mabie, Z. Zang, L. Santschi, and J. A. Kessler. 1996. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17: 595–606.
   PubMed Web of Science ®Google Scholar
• Gurdon, J. B., P. Harger, A. Mitchell, and P. Lemaire. 1994. Activin signalling and response to a morphogen gradient. Nature 371: 487–492.
   PubMedGoogle Scholar
• Hayashi, H., S. Abdollah, Y. Qiu, J. Cai, Y. Y. Xu, B. W. Grinnell, M. A. Richardson, J. N. Topper, M. A. Gimbrone, Jr., J. L. Wrana, and D. Falb. 1997. The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 89: 1165–1173.
   PubMed Web of Science ®Google Scholar
• Hogan, B. L. 1996. Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6: 432–438.
   PubMed Web of Science ®Google Scholar
• Hogan, B. L. 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10: 1580–1594.
   PubMed Web of Science ®Google Scholar
• Imamura, T., M. Takase, A. Nishihara, E. Oeda, J. Hanai, M. Kawabata, and K. Miyazono. 1997. Smad6 inhibits signalling by the TGF-β superfamily. Nature 389: 622–626.
   PubMed Web of Science ®Google Scholar
• Ishisaki, A., K. Yamato, S. Hashimoto, A. Nakao, K. Tamaki, K. Nonaka, P. ten Dijke, H. Sugino, and T. Nishihara. 1999. Differential inhibition of Smad6 and Smad7 on bone morphogenetic protein- and activin-mediated growth arrest and apoptosis in B cells. J. Biol. Chem. 274: 13637–13642.
   PubMedGoogle Scholar
• Ishisaki, A., K. Yamato, A. Nakao, K. Nonaka, M. Ohguchi, P. ten Dijke, and T. Nishihara. 1998. Smad7 is an activin-inducible inhibitor of activin-induced growth arrest and apoptosis in mouse B cells. J. Biol. Chem. 273: 24293–24296.
   PubMed Web of Science ®Google Scholar
• Jena, N., C. Martin-Seisdedos, P. McCue, and C. M. Croce. 1997. BMP7 null mutation in mice: developmental defects in skeleton, kidney, and eye. Exp. Cell Res. 230: 28–37.
   PubMed Web of Science ®Google Scholar
• Kaiser, D., M. A. Freyberg, and P. Friedl. 1997. Lack of hemodynamic forces triggers apoptosis in vascular endothelial cells. Biochem. Biophys. Res. Commun. 231: 586–590.
   PubMed Web of Science ®Google Scholar
• Karsenty, G., G. Luo, C. Hofmann, and A. Bradley. 1996. BMP 7 is required for nephrogenesis, eye development, and skeletal patterning. Ann. N. Y. Acad. Sci. 785: 98–107.
   PubMed Web of Science ®Google Scholar
• Kim, H. S., M. Aikawa, K. Kimura, M. Kuro-o, K. Nakahara, T. Suzuki, H. Katoh, E. Okamoto, Y. Yazaki, and R. Nagai. 1993. Ductus arteriosus. Advanced differentiation of smooth muscle cells demonstrated by myosin heavy chain isoform expression in rabbits. Circulation 88: 1804–1810.
   PubMedGoogle Scholar
• Kretzschmar, M., F. Liu, A. Hata, J. Doody, and J. Massague. 1997. The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11: 984–995.
   PubMedGoogle Scholar
• Lang, R., M. Lustig, F. Francois, M. Sellinger, and H. Plesken. 1994. Apoptosis during macrophage-dependent ocular tissue remodelling. Development 120: 3395–3403.
   PubMedGoogle Scholar
• Liu, F., A. Hata, J. C. Baker, J. Doody, J. Carcamo, R. M. Harland, and J. Massague. 1996. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381: 620–623.
   PubMed Web of Science ®Google Scholar
• Luo, G., C. Hofmann, A. L. Bronckers, M. Sohocki, A. Bradley, and G. Karsenty. 1995. BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev. 9: 2808–2820.
   PubMed Web of Science ®Google Scholar
• Macias, D., Y. Ganan, T. K. Sampath, M. E. Piedra, M. A. Ros, and J. M. Hurle. 1997. Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development 124: 1109–1117.
   PubMed Web of Science ®Google Scholar
• Maisonpierre, P. C., C. Suri, P. F. Jones, S. Bartunkova, S. J. Wiegand, C. Radziejewski, D. Compton, J. McClain, T. H. Aldrich, N. Papadopoulos, T. J. Daly, S. Davis, T. N. Sato, and G. D. Yancopoulos. 1997. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55–60.
   PubMed Web of Science ®Google Scholar
• Marazzi, G., Y. Wang, and D. Sassoon. 1997. Msx2 is a transcriptional regulator in the BMP4-mediated programmed cell death pathway. Dev. Biol. 186: 127–138.
   PubMedGoogle Scholar
• Meeson, A. P., M. Argilla, K. Ko, L. Witte, and R. A. Lang. 1999. VEGF deprivation-induced apoptosis is a component of programmed capillary regression. Development 126: 1407–1415.
   PubMed Web of Science ®Google Scholar
• Mehler, M. F., P. C. Mabie, D. Zhang, and J. A. Kessler. 1997. Bone morphogenetic proteins in the nervous system. Trends Neurosci. 20: 309–317.
   PubMedGoogle Scholar
• Nakao, A., M. Afrakhte, A. Moren, T. Nakayama, J. L. Christian, R. Heuchel, S. Itoh, M. Kawabata, N. E. Heldin, C. H. Heldin, and P. ten Dijke. 1997. Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 389: 631–635.
   PubMed Web of Science ®Google Scholar
• Nellen, D., R. Burke, G. Struhl, and K. Basler. 1996. Direct and long-range action of a DPP morphogen gradient. Cell 85: 357–368.
   PubMed Web of Science ®Google Scholar
• Neumann, C., and S. Cohen. 1997. Morphogens and pattern formation. Bioessays 19: 721–729.
   PubMed Web of Science ®Google Scholar
• Pollman, M. J., L. Naumovski, and G. H. Gibbons. 1999. Endothelial cell apoptosis in capillary network remodeling. J. Cell. Physiol. 178: 359–370.
   PubMed Web of Science ®Google Scholar
• Resnick, N., and M. A. Gimbrone, Jr. 1995. Hemodynamic forces are complex regulators of endothelial gene expression. FASEB J. 9: 874–882.
   PubMed Web of Science ®Google Scholar
• Rong, P., A. M. Bennie, W. R. Epa, and G. L. Barrett. 1999. Nerve growth factor determines survival and death of PC12 cells by regulation of the bcl-x, bax, and caspase-3 genes. J. Neurochem. 72: 2294–2300.
   PubMedGoogle Scholar
• Ruoslahti, E., and J. C. Reed. 1994. Anchorage dependence, integrins, and apoptosis. Cell 77: 477–478.
   PubMed Web of Science ®Google Scholar
• Trousse, F., P. Esteve, and P. Bovolenta. 2001. Bmp4 mediates apoptotic cell death in the developing chick eye. J. Neurosci. 21: 1292–1301.
   PubMedGoogle Scholar
• Vainio, S., I. Karavanova, A. Jowett, and I. Thesleff. 1993. Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75: 45–58.
   PubMed Web of Science ®Google Scholar
• Whitman, M. 1998. Smads and early developmental signaling by the TGFβ superfamily. Genes Dev. 12: 2445–2462.
   PubMed Web of Science ®Google Scholar
• Ying, Y., and G. Q. Zhao. 2000. Detection of multiple bone morphogenetic protein messenger ribonucleic acids and their signal transducer, Smad1, during mouse decidualization. Biol. Reprod. 63: 1781–1786.
   PubMed Web of Science ®Google Scholar
• Zou, H., and L. Niswander. 1996. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 272: 738–741.
   PubMed Web of Science ®Google Scholar