A Novel Regulatory Mechanism of the Bone Morphogenetic Protein (BMP) Signaling Pathway Involving the Carboxyl-Terminal Tail Domain of BMP Type II Receptor

REFERENCES

• Abdalla, S. A., C. J. Gallione, R. J. Barst, E. M. Horn, J. A. Knowles, D. A. Marchuk, M. Letarte, and J. H. Morse. 2004. Primary pulmonary hypertension in families with hereditary haemorrhagic telangiectasia. Eur. Respir. J. 23:373–377.
   PubMed Web of Science ®Google Scholar
• Attisano, L., and S. Tuen Lee-Hoeflich. 2001. The Smads. Genome Biol. 2:REVIEWS3010.
   PubMedGoogle Scholar
• Attisano, L., and J. L. Wrana. 2002. Signal transduction by the TGFβ superfamily. Science 296:1646–1647.
   PubMed Web of Science ®Google Scholar
• Beppu, H., F. Ichinose, N. Kawai, R. C. Jones, P. B. Yu, W. M. Zapol, K. Miyazono, E. Li, and K. D. Bloch. 2004. BMPR-II heterozygous mice have mild pulmonary hypertension and an impaired pulmonary vascular remodeling response to prolonged hypoxia. Am. J. Physiol. Lung Cell. Mol. Physiol. 287:L1241–L1247.
   PubMedGoogle Scholar
• Bowers, A. J., S. Scully, and J. F. Boylan. 2003. SKIP3, a novel Drosophila tribbles ortholog, is overexpressed in human tumors and is regulated by hypoxia. Oncogene 22:2823–2835.
   PubMedGoogle Scholar
• Cárcamo, J., F. M. B. Weis, F. Ventura, R. Wieser, J. L. Wrana, L. Attisano, and J. Massagué. 1994. Type I receptors specify growth inhibitory and transcriptional responses to TGFβ and activin. Mol. Cell. Biol. 14:3810–3821.
   PubMed Web of Science ®Google Scholar
• Derynck, R., and Y. E. Zhang. 2003. Smad-dependent and Smad-independent pathways in TGFβ family signalling. Nature 425:577–584.
   PubMed Web of Science ®Google Scholar
• Du, K., S. Herzig, R. N. Kulkarni, and M. Montminy. 2003. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300:1574–1577.
   PubMed Web of Science ®Google Scholar
• Ebisawa, T., M. Fukuchi, G. Murakami, T. Chiba, K. Tanaka, T. Imamura, and K. Miyazono. 2001. Smurf1 interacts with transforming growth factor-β type I receptor through Smad7 and induces receptor degradation. J. Biol. Chem. 276:12477–12480.
   PubMed Web of Science ®Google Scholar
• Eddahibi, S., N. Morrell, M. P. d'Ortho, R. Naeije, and S. Adnot. 2002. Pathobiology of pulmonary arterial hypertension. Eur. Respir. J. 20:1559–1572.
   PubMed Web of Science ®Google Scholar
• Estevez, M., L. Attisano, J. L. Wrana, P. S. Albert, J. Massagué, and D. L. Riddle. 1993. The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans larva development. Nature 365:644–649.
   PubMedGoogle Scholar
• Foletta, V. C., M. A. Lim, J. Soosairajah, A. P. Kelly, E. G. Stanley, M. Shannon, W. He, S. Das, J. Massague, and O. Bernard. 2003. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J. Cell Biol. 162:1089–1098.
   PubMed Web of Science ®Google Scholar
• Fujii, M., K. Takeda, T. Imamura, H. Aoki, T. K. Smapath, S. Enomoto, M. Kawabata, M. Kato, H. Ichijo, and K. Miyazono. 1999. Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol. Biol. Cell 10:3801–3813.
   PubMed Web of Science ®Google Scholar
• Grosshans, J., and E. Wieschaus. 2000. A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101:523–531.
   PubMed Web of Science ®Google Scholar
• Harral, J., and J. West. 2006. Mice expressing BMPR2(R899X) transgene develop pulmonary vascular lesions, p. 89. Abstr. Evol. Pulm. Hypertens. Emerg. Dis. Novel Ther., National Institute of Health, Bethesda, MD, 7 to 8 December 2006.
   Google Scholar
• Hartung, A., K. Bitton-Worms, M. M. Rechtman, V. Wenzel, J. H. Boergermann, S. Hassel, Y. I. Henis, and P. Knaus. 2006. Different routes of bone morphogenic protein (BMP) receptor endocytosis influence BMP signaling. Mol. Cell. Biol. 26:7791–7805.
   PubMed Web of Science ®Google Scholar
• Hata, A., J. Seoane, G. Lagna, E. Montalvo, A. Hemmati-Brivanlou, and J. Massague. 2000. OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways. Cell 100:229–240.
   PubMed Web of Science ®Google Scholar
• Hegedus, Z., A. Czibula, and E. Kiss-Toth. 2006. Tribbles: novel regulators of cell function; evolutionary aspects. Cell. Mol. Life Sci. 63:1632–1641.
   PubMedGoogle Scholar
• Hicke, L. 2001. Protein regulation by monoubiqutin. Nat. Rev. Mol. Cell Biol. 2:195–201.
   PubMed Web of Science ®Google Scholar
• Hogan, B. L., M. Blessing, G. E. Winnier, N. Suzuki, and C. M. Jones. 1994. Growth factors in development: the role of TGFβ related polypeptide signalling molecules in embryogenesis. Dev. Suppl. 1994:53–60.
   Google Scholar
• Hogan, B. L. M. 1996. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10:1580–1594.
   PubMed Web of Science ®Google Scholar
• Ishikawa, T., H. Yoshioka, H. Ohuchi, S. Noji, and T. Nohno. 1995. Truncated type II receptor for BMP-4 induces secondary axial structures in Xenopus embryos. Biochem. Biophys. Res. Commun. 216:26–33.
   PubMedGoogle Scholar
• Katagiri, T., A. Yamaguchi, M. Komaki, E. Abe, N. Takahashi, T. Ikeda, V. Rosen, J. M. Wozney, A. Fujisawa-Sehara, and T. Suda. 1994. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage J. Cell Biol. 127:1755–1766.
   PubMed Web of Science ®Google Scholar
• Kato, S., and K. Du. 2007. TRB3 modulates C2C12 differentiation by interfering with Akt activation. Biochem. Biophys. Res. Commun. 353:933–938.
   PubMed Web of Science ®Google Scholar
• Lagna, G., P. H. Nguyen, W. Ni, and A. Hata. 2006. BMP-dependent activation of caspase-9 and caspase-8 mediates apoptosis in pulmonary artery smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 291:1059–1067.
   Google Scholar
• Lee-Hoeflich, S. T., C. G. Causing, M. Podkowa, X. Zhao, J. L. Wrana, and L. Attisano. 2004. Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis. EMBO J. 23:4792–4801.
   PubMedGoogle Scholar
• Letsou, A., K. Arora, J. L. Wrana, K. Simin, V. Twombly, J. Jamal, K. Staehling-Hampton, F. M. Hoffmann, W. M. Gelbart, J. Massagué, and M. B. O'Connor. 1995. Drosophila dpp signaling is mediated by the punt gene product: a dual ligand binding type II receptor of the TGFβ receptor family. Cell 80:899–908.
   PubMedGoogle Scholar
• Loirand, G., P. Guerin, and P. Pacaud. 2006. Rho kinases in cardiovascular physiology and pathophysiology. Circ. Res. 98:322–334.
   PubMed Web of Science ®Google Scholar
• Machado, R. D., M. W. Pauciulo, J. R. Thomson, K. B. Lane, N. V. Morgan, L. Wheeler, J. A. Phillips III, J. Newman, D. Williams, N. Galie, A. Manes, K. McNeil, M. Yacoub, G. Mikhail, P. Rogers, P. Corris, M. Humbert, D. Donnai, G. Martensson, L. Tranebjaerg, J. E. Loyd, R. C. Trembath, and W. C. Nichols. 2001. BMPR2 haploinsufficiency as the inherited molecular mechanism for primary pulmonary hypertension. Am. J. Hum. Genet. 68:92–102.
   PubMed Web of Science ®Google Scholar
• Machado, R. D., N. Rudarakanchana, C. Atkinson, J. A. Flanagan, R. Harrison, N. W. Morrell, and R. C. Trembath. 2003. Functional interaction between BMPR-II and Tctex-1, a light chain of Dynein, is isoform-specific and disrupted by mutations underlying primary pulmonary hypertension. Hum. Mol. Genet. 12:3277–3286.
   PubMedGoogle Scholar
• Massagué, J. 1998. TGFβ signal transduction. Annu. Rev. Biochem. 67:753–791.
   PubMed Web of Science ®Google Scholar
• Massague, J., J. Seoane, and D. Wotton. 2005. Smad transcription factors. Genes Dev. 19:2783–2810.
   PubMed Web of Science ®Google Scholar
• Mata, J., S. Curado, A. Ephrussi, and P. Rorth. 2000. Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101:511–522.
   PubMed Web of Science ®Google Scholar
• Mayumi-Matsuda, K., S. Kojima, H. Suzuki, and T. Sakata. 1999. Identification of a novel kinase-like gene induced during neuronal cell death. Biochem. Biophys. Res. Commun. 258:260–264.
   PubMed Web of Science ®Google Scholar
• Mehra, A., and J. L. Wrana. 2002. TGFβ and the Smad signal transduction pathway. Biochem. Cell Biol. 80:605–622.
   PubMed Web of Science ®Google Scholar
• Murakami, G., T. Watabe, K. Takaoka, K. Miyazono, and T. Imamura. 2003. Cooperative inhibition of bone morphogenetic protein signaling by Smurf1 and inhibitory Smads. Mol. Biol. Cell 14:2809–2817.
   PubMed Web of Science ®Google Scholar
• Naeije, R., and B. Rondelet. 2004. Pathobiology of pulmonary arterial hypertension. Bull. Mem. Acad. R. Med. Belg. 159:219–226.
   PubMedGoogle Scholar
• Nishihara, A., T. Watabe, T. Imamura, and K. Miyazono. 2002. Functional heterogeneity of bone morphogenetic protein receptor-II mutants found in patients with primary pulmonary hypertension. Mol. Biol. Cell 13:3055–3063.
   PubMedGoogle Scholar
• Ohoka, N., S. Yoshii, T. Hattori, K. Onozaki, and H. Hayashi. 2005. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 24:1243–1255.
   PubMed Web of Science ®Google Scholar
• Ord, D., and T. Ord. 2003. Mouse NIPK interacts with ATF4 and affects its transcriptional activity. Exp. Cell Res. 286:308–320.
   PubMedGoogle Scholar
• Pacaud, P., V. Sauzeau, and G. Loirand. 2005. Rho proteins and vascular diseases. Arch. Mal. Coeur Vaiss. 98:249–254.
   PubMedGoogle Scholar
• Qi, L., J. E. Heredia, J. Y. Altarejos, R. Screaton, N. Goebel, S. Niessen, I. X. Macleod, C. W. Liew, R. N. Kulkarni, J. Bain, C. Newgard, M. Nelson, R. M. Evans, J. Yates, and M. Montminy. 2006. TRB3 links the E3 ubiquitin ligase COP1 to lipid metabolism. Science 312:1763–1766.
   PubMed Web of Science ®Google Scholar
• Rorth, P., K. Szabo, and G. Texido. 2000. The level of C/EBP protein is critical for cell migration during Drosophila oogenesis and is tightly controlled by regulated degradation. Mol. Cell 6:23–30.
   PubMed Web of Science ®Google Scholar
• Rubin, L. J., and S. Rich. 1997. Primary pulmonary hypertension. Marcel Dekker, Inc., New York, NY.
   Google Scholar
• Schulz, C., A. A. Kiger, S. I. Tazuke, Y. M. Yamashita, L. C. Pantalena-Filho, D. L. Jones, C. G. Wood, and M. T. Fuller. 2004. A misexpression screen reveals effects of bag-of-marbles and TGFβ class signaling on the Drosophila male germ-line stem cell lineage. Genetics 167:707–723.
   PubMed Web of Science ®Google Scholar
• Seher, T. C., and M. Leptin. 2000. Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila gastrulation. Curr. Biol. 10:623–629.
   PubMedGoogle Scholar
• Thomson, J. R., R. D. Machado, M. W. Pauciulo, N. V. Morgan, M. Humbert, G. C. Elliott, K. Ward, M. Yacoub, G. Mikhail, P. Rogers, J. Newman, L. Wheeler, T. Higenbottam, J. S. Gibbs, J. Egan, A. Crozier, A. Peacock, R. Allcock, P. Corris, J. E. Loyd, R. C. Trembath, and W. C. Nichols. 2000. Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-beta family. J. Med. Genet. 37:741–745.
   PubMed Web of Science ®Google Scholar
• Wang, H. R., Y. Zhang, B. Ozdamar, A. A. Ogunjimi, E. Alexandrova, G. H. Thomsen, and J. L. Wrana. 2003. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302:1775–1779.
   PubMed Web of Science ®Google Scholar
• West, J., K. Fagan, W. Steudel, B. Fouty, K. Lane, J. Harral, M. Hoedt-Miller, Y. Tada, J. Ozimek, R. Tuder, and D. M. Rodman. 2004. Pulmonary hypertension in transgenic mice expressing a dominant-negative BMPRII gene in smooth muscle. Circ. Res. 94:1109–1114.
   PubMed Web of Science ®Google Scholar
• Ying, S. X., Z. J. Hussain, and Y. E. Zhang. 2003. Smurf1 facilitates myogenic differentiation and antagonizes the bone morphogenetic protein-2-induced osteoblast conversion by targeting Smad5 for degradation. J. Biol. Chem. 278:39029–39036.
   PubMed Web of Science ®Google Scholar
• Zhang, S., I. Fantozzi, D. D. Tigno, E. S. Yi, O. Platoshyn, P. A. Thistlethwaite, J. M. Kriett, G. Yung, L. J. Rubin, and J. X. Yuan. 2003. Bone morphogenetic proteins induce apoptosis in human pulmonary vascular smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 285:L740–L754.
   PubMed Web of Science ®Google Scholar
• Zhu, H., P. Kavsak, S. Abdollah, J. L. Wrana, and G. H. Thomsen. 1999. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400:687–693.
   PubMed Web of Science ®Google Scholar