Adult-Specific Systemic Over-Expression Reveals Novel In Vivo Effects of the Soluble Forms of ActRIIA, ActRIIB and BMPRII

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Yamawaki, Kengo ^a   Ueda, Shinobu ^b   Okada, Tsutomu ^a   Oshima, Takeshi ^a   Kakitani, Makoto ^a   Kato, Takashi ^b   Tomizuka, Kazuma ^a  

^a KYOWA HAKKO KOGYO CO LTD   (Japan)

^b WASEDA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 2; BONE MORPHOGENETIC PROTEIN RECEPTOR 2A; BONE MORPHOGENETIC PROTEIN RECEPTOR 2B; HYBRID PROTEIN; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G1; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL VIABILITY; CHIMERA; CONTROLLED STUDY; ERYTHROCYTE; EXTRAMEDULLARY HEMATOPOIESIS; FEMALE; FLOW CYTOMETRY; HISTOLOGY; MALE; MOUSE; NONHUMAN; PHENOTYPE; SPLEEN; TRANSGENE; TRANSGENIC MOUSE;

ACTIVIN RECEPTORS, TYPE II; ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; ERYTHROCYTES; ERYTHROPOIETIN; FLOW CYTOMETRY; HUMANS; MICE, KNOCKOUT; MICE, TRANSGENIC;

EID: 84886897989     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078076     Document Type: Article

References (55)

1. Feng XH, Derynck R, (2005) Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 21: 659-693. doi:10.1146/annurev.cellbio.21.022404.142018. PubMed: 16212511.
2. Massagué J, (1998) TGF-beta signal transduction. Annu Rev Biochem 67: 753-791. doi:10.1146/annurev.biochem.67.1.753. PubMed: 9759503.
3. Chang H, Brown CW, Matzuk MM, (2002) Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr Rev 23: 787-823. doi:10.1210/er.2002-0003. PubMed: 12466190.
4. Zhao GQ, (2003) Consequences of knocking out BMP signaling in the mouse. Genesis 35: 43-56. doi:10.1002/gene.10167. PubMed: 12481298.
5. Kitisin K, Saha T, Blake T, Golestaneh N, Deng M, et al. (2007) Tgf-beta signaling in development. Sci STKE(2007): pp. cm1. PubMed: 17699101.
6. Lowery JW, de Caestecker MP, (2010) BMP signaling in vascular development and disease. Cytokine Growth Factor Rev 21: 287-298. doi:10.1016/j.cytogfr.2010.06.001. PubMed: 20674464.
7. Cai J, Pardali E, Sánchez-Duffhues G, ten Dijke P, (2012) BMP signaling in vascular diseases. FEBS Lett 586: 1993-2002. doi:10.1016/j.febslet.2012.04.030. PubMed: 22710160.
8. McPherron AC, Lawler AM, Lee SJ, (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387: 83-90. doi:10.1038/387083a0. PubMed: 9139826.
9. Zhang H, Bradley A, (1996) Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122: 2977-2986. PubMed: 8898212.
10. Jiao K, Kulessa H, Tompkins K, Zhou Y, Batts L, et al. (2003) An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev 17: 2362-2367. doi:10.1101/gad.1124803. PubMed: 12975322.
11. Chen H, Shi S, Acosta L, Li W, Lu J, et al. (2004) BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131: 2219-2231. doi:10.1242/dev.01094. PubMed: 15073151.
12. Goldman DC, Hackenmiller R, Nakayama T, Sopory S, Wong C, et al. (2006) Mutation of an upstream cleavage site in the BMP4 prodomain leads to tissue-specific loss of activity. Development 133: 1933-1942. doi:10.1242/dev.02368. PubMed: 16624858.
13. Zhao GQ, Chen YX, Liu XM, Xu Z, Qi X, (2001) Mutation in Bmp7 exacerbates the phenotype of Bmp8a mutants in spermatogenesis and epididymis. Dev Biol 240: 212-222. doi:10.1006/dbio.2001.0448. PubMed: 11784057.
14. Meynard D, Kautz L, Darnaud V, Canonne-Hergaux F, Coppin H, et al. (2009) Lack of the bone morphogenetic protein BMP6 induces massive iron overload. Nat Genet 41: 478-481. doi:10.1038/ng.320. PubMed: 19252488.
15. Zhang J, Niu C, Ye L, Huang H, He X, et al. (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425: 836-841. doi:10.1038/nature02041. PubMed: 14574412.
16. Burton VJ, Ciuclan LI, Holmes AM, Rodman DM, Walker C, et al. (2011) Bone morphogenetic protein receptor II regulates pulmonary artery endothelial cell barrier function. Blood 117: 333-341. doi:10.1182/blood-2010-05-285973. PubMed: 20724539.
17. Murali D, Yoshikawa S, Corrigan RR, Plas DJ, Crair MC, et al. (2005) Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development 132: 913-923. doi:10.1242/dev.01673. PubMed: 15673568.
18. Yoon BS, Ovchinnikov DA, Yoshii I, Mishina Y, Behringer RR, et al. (2005) Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc Natl Acad Sci U S A 102: 5062-5067. doi:10.1073/pnas.0500031102. PubMed: 15781876.
19. Bagarova J, Vonner AJ, Armstrong KA, Börgermann J, Lai CSC, et al. (2013) Constitutively Active ALK2 Receptor Mutants Require Type II Receptor Cooperation. Mol Cell Biol 33: 2413-2424. doi:10.1128/MCB.01595-12. PubMed: 23572558.
20. Mazerbourg S, Sangkuhl K, Luo CW, Sudo S, Klein C, et al. (2005) Identification of receptors and signaling pathways for orphan bone morphogenetic protein/growth differentiation factor ligands based on genomic analyses. J Biol Chem 280: 32122-32132. doi:10.1074/jbc.M504629200. PubMed: 16049014.
21. Heinecke K, Seher A, Schmitz W, Mueller TD, Sebald W, et al. (2009) Receptor oligomerization and beyond: a case study in bone morphogenetic proteins. BMC Biol 7: 59. doi:10.1186/1741-7007-7-59. PubMed: 19735544.
22. Shimasaki S, Moore RK, Otsuka F, Erickson GF, (2004) The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25: 72-101. doi:10.1210/er.2003-0007. PubMed: 14769828.
23. Mueller TD, Nickel J, (2012) Promiscuity and specificity in BMP receptor activation. FEBS Lett 586: 1846-1859. doi:10.1016/j.febslet.2012.02.043. PubMed: 22710174.
24. Chantry AD, Heath D, Mulivor AW, Pearsall S, Baud'huin M, et al. (2010) Inhibiting activin-A signaling stimulates bone formation and prevents cancer-induced bone destruction in vivo. J Bone Miner Res 25: 2633-2646. doi:10.1002/jbmr.142. PubMed: 20533325.
25. Lee SJ, Reed LA, Davies MV, Girgenrath S, Goad ME, et al. (2005) Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc Natl Acad Sci U S A 102: 18117-18122. doi:10.1073/pnas.0505996102. PubMed: 16330774.
26. Koncarevic A, Cornwall-Brady M, Pullen A, Davies M, Sako D, et al. (2010) A soluble activin receptor type IIb prevents the effects of androgen deprivation on body composition and bone health. Endocrinology 151: 4289-4300. doi:10.1210/en.2010-0134. PubMed: 20573726.
27. Kakitani M, Oshima T, Horikoshi K, Yoshitome T, Ueda A, et al. (2005) A novel transgenic chimaeric mouse system for the rapid functional evaluation of genes encoding secreted proteins. Nucleic Acids Res 33: e85. doi:10.1093/nar/gki353. PubMed: 15914664.
28. Kim KA, Kakitani M, Zhao J, Oshima T, Tang T, et al. (2005) Mitogenic influence of human R-spondin1 on the intestinal epithelium. Science 309: 1256-1259. doi:10.1126/science.1112521. PubMed: 16109882.
29. Gorman JR, van der Stoep N, Monroe R, Cogne M, Davidson L, et al. (1996) The Ig(kappa) enhancer influences the ratio of Ig(kappa) versus Ig(lambda) B lymphocytes. Immunity 5: 241-252. doi:10.1016/S1074-7613(00)80319-2. PubMed: 8808679.
30. Dal Canto MC, Gurney ME, (1997) A low expressor line of transgenic mice carrying a mutant human Cu,Zn superoxide dismutase (SOD1) gene develops pathological changes that most closely resemble those in human amyotrophic lateral sclerosis. Acta Neuropathol 93: 537-550. doi:10.1007/s004010050650. PubMed: 9194892.
31. Raje N, Vallet S, (2010) Sotatercept, a soluble activin receptor type 2A IgG-Fc fusion protein for the treatment of anemia and bone loss. Curr Opin Mol Ther 12: 586-597. PubMed: 20886391.
32. Lane KB, Machado RD, Pauciulo MW, Thomson JR, Phillips JA III, et al. (2000) Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. Nat Genet 26: 81-84. doi:10.1038/79226. PubMed: 10973254.
33. Machado RD, Aldred MA, James V, Harrison RE, Patel B, et al. (2006) Mutations of the TGF-beta type II receptor BMPR2 in pulmonary arterial hypertension. Hum Mutat 27: 121-132. doi:10.1002/humu.20285. PubMed: 16429395.
34. Johnson DW, Berg JN, Baldwin MA, Gallione CJ, Marondel I, et al. (1996) Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat Genet 13: 189-195. doi:10.1038/ng0696-189. PubMed: 8640225.
35. Liu D, Wang J, Kinzel B, Müeller M, Mao X, et al. (2007) Dosage-dependent requirement of BMP type II receptor for maintenance of vascular integrity. Blood 110: 1502-1510. doi:10.1182/blood-2006-11-058594. PubMed: 17496203.
36. Brown MA, Zhao Q, Baker KA, Naik C, Chen C, et al. (2005) Crystal structure of BMP-9 and functional interactions with pro-region and receptors. J Biol Chem 280: 25111-25118. doi:10.1074/jbc.M503328200. PubMed: 15851468.
37. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S, (2007) Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 109: 1953-1961. doi:10.1182/blood-2006-07-034124. PubMed: 17068149.
38. Scharpfenecker M, van Dinther M, Liu Z, van Bezooijen RL, Zhao Q, et al. (2007) BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J Cell Sci 120: 964-972. doi:10.1242/jcs.002949. PubMed: 17311849.
39. Souza TA, Chen X, Guo Y, Sava P, Zhang J, et al. (2008) Proteomic identification and functional validation of activins and bone morphogenetic protein 11 as candidate novel muscle mass regulators. Mol Endocrinol 22: 2689-2702. doi:10.1210/me.2008-0290. PubMed: 18927237.
40. He XC, Zhang J, Tong WG, Tawfik O, Ross J, et al. (2004) BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet 36: 1117-1121. doi:10.1038/ng1430. PubMed: 15378062.
41. Auclair BA, Benoit YD, Rivard N, Mishina Y, Perreault N, (2007) Bone morphogenetic protein signaling is essential for terminal differentiation of the intestinal secretory cell lineage. Gastroenterology 133: 887-896. doi:10.1053/j.gastro.2007.06.066. PubMed: 17678919.
42. Daluiski A, Engstrand T, Bahamonde ME, Gamer LW, Agius E, et al. (2001) Bone morphogenetic protein-3 is a negative regulator of bone density. Nat Genet 27: 84-88. doi:10.1038/87280. PubMed: 11138004.
43. Zouvelou V, Luder HU, Mitsiadis TA, Graf D, (2009) Deletion of BMP7 affects the development of bones, teeth, and other ectodermal appendages of the orofacial complex. J Exp Zool B Mol Dev Evol 312B: 361-374. doi:10.1002/jez.b.21262. PubMed: 19127565.
44. Gluhak-Heinrich J, Guo D, Yang W, Harris MA, Lichtler A, et al. (2010) New roles and mechanism of action of BMP4 in postnatal tooth cytodifferentiation. Bone 46: 1533-1545. doi:10.1016/j.bone.2010.02.024. PubMed: 20206312.
45. Lee SJ, McPherron AC, (2001) Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci U S A 98: 9306-9311. doi:10.1073/pnas.151270098. PubMed: 11459935.
46. Rebbapragada A, Benchabane H, Wrana JL, Celeste AJ, Attisano L, (2003) Myostatin signals through a transforming growth factor beta-like signaling pathway to block adipogenesis. Mol Cell Biol 23: 7230-7242. doi:10.1128/MCB.23.20.7230-7242.2003. PubMed: 14517293.
47. Fields SZ, Parshad S, Anne M, Raftopoulos H, Alexander MJ, et al. (2013) Activin receptor antagonists for cancer-related anemia and bone disease. Expert Opin Investig Drugs 22: 87-101. doi:10.1517/13543784.2013.738666. PubMed: 23127248.
48. Sako D, Grinberg AV, Liu J, Davies MV, Castonguay R, et al. (2010) Characterization of the ligand binding functionality of the extracellular domain of activin receptor type IIb. J Biol Chem 285: 21037-21048. doi:10.1074/jbc.M110.114959. PubMed: 20385559.
49. Millot S, Andrieu V, Letteron P, Lyoumi S, Hurtado-Nedelec M, et al. (2010) Erythropoietin stimulates spleen BMP4-dependent stress erythropoiesis and partially corrects anemia in a mouse model of generalized inflammation. Blood 116: 6072-6081. doi:10.1182/blood-2010-04-281840. PubMed: 20844235.
50. Lenox LE, Shi L, Hegde S, Paulson RF, (2009) Extramedullary erythropoiesis in the adult liver requires BMP-4/Smad5-dependent signaling. Exp Hematol 37: 549-558. doi:10.1016/j.exphem.2009.01.004. PubMed: 19375646.
51. Wu MY, Hill CS, (2009) Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev Cell 16: 329-343. doi:10.1016/j.devcel.2009.02.012. PubMed: 19289080.
52. de Caestecker M, (2004) The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev 15: 1-11. doi:10.1016/j.cytogfr.2003.10.004. PubMed: 14746809.
53. Blank U, Seto ML, Adams DC, Wojchowski DM, Karolak MJ, et al. (2008) An in vivo reporter of BMP signaling in organogenesis reveals targets in the developing kidney. BMC Dev Biol 8: 86. doi:10.1186/1471-213X-8-86. PubMed: 18801194.
54. Javier AL, Doan LT, Luong M, Reyes de Mochel NS, Sun A, et al. (2012) Bmp indicator mice reveal dynamic regulation of transcriptional response. PLOS ONE 7: e42566. doi:10.1371/journal.pone.0042566. PubMed: 22984405.
55. Tomizuka K, Shinohara T, Yoshida H, Uejima H, Ohguma A, et al. (2000) Double trans-chromosomic mice: maintenance of two individual human chromosome fragments containing Ig heavy and kappa loci and expression of fully human antibodies. Proc Natl Acad Sci U S A 97: 722-727. doi:10.1073/pnas.97.2.722. PubMed: 10639146.