The role of bone morphogenetic proteins in myeloma cell survival

Cytokine and Growth Factor Reviews

Volumn 25, Issue 3, 2014, Pages 343-350

  Holien, Toril ^a   Sundan, Anders ^a,b  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Apoptosis; BMP; Bone morphogenetic protein; Multiple myeloma

Indexed keywords

ANTINEOPLASTIC AGENT; BONE MORPHOGENETIC PROTEIN; DORSOMORPHIN; HEPCIDIN; INTERLEUKIN 3; PROTEIN CDC25; PROTEIN TYROSINE PHOSPHATASE; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; TUMOR PROTEIN;

ANEMIA; APOPTOSIS; BINDING AFFINITY; BONE DISEASE; CELL CYCLE ARREST; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; DRUG MECHANISM; DRUG TARGETING; ENDOCYTOSIS; GROWTH INHIBITION; HOMEOSTASIS; HUMAN; LIGAND BINDING; MYELOMA; MYELOMA CELL; NONHUMAN; OSTEOBLAST; OSTEOPOROSIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TARGETING; SHORT SURVEY; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; METABOLISM; MULTIPLE MYELOMA; PATHOLOGY;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEINS; CELL SURVIVAL; HUMANS; MODELS, BIOLOGICAL; MULTIPLE MYELOMA; NEOPLASM PROTEINS; SIGNAL TRANSDUCTION;

EID: 84902076173     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2014.04.009     Document Type: Short Survey

References (100)

1. Hogan B.L. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 1996, 10:1580-1594.
2. Bragdon B., Moseychuk O., Saldanha S., King D., Julian J., Nohe A. Bone morphogenetic proteins: a critical review. Cell Signal 2011, 23:609-620.
3. Wakefield L.M., Hill C.S. Beyond TGFbeta: roles of other TGFbeta superfamily members in cancer. Nat Rev Cancer 2013, 13:328-341.
4. Palumbo A., Anderson K. Multiple myeloma. N Engl J Med 2011, 364:1046-1060.
5. Urist M.R. Bone: formation by autoinduction. Science 1965, 150:893-899.
6. Wozney J.M., Rosen V., Celeste A.J., Mitsock L.M., Whitters M.J., Kriz R.W., et al. Novel regulators of bone formation: molecular clones and activities. Science 1988, 242:1528-1534.
7. Massague J. TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 1996, 85:947-950.
8. Oh S.P., Seki T., Goss K.A., Imamura T., Yi Y., Donahoe P.K., et al. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci U S A 2000, 97:2626-2631.
9. Goumans M.J., Valdimarsdottir G., Itoh S., Lebrin F., Larsson J., Mummery C., et al. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol Cell 2003, 12:817-828.
10. Upton P.D., Davies R.J., Trembath R.C., Morrell N.W. Bone morphogenetic protein (BMP) and activin type II receptors balance BMP9 signals mediated by activin receptor-like kinase-1 in human pulmonary artery endothelial cells. J Biol Chem 2009, 284:15794-15804.
11. Holtzhausen A., Golzio C., How T., Lee Y.H., Schiemann W.P., Katsanis N., et al. Novel bone morphogenetic protein signaling through Smad2 and Smad3 to regulate cancer progression and development. FASEB J 2013, 28:1248-1267.
12. Rejon C.A., Hancock M.A., Li Y.N., Thompson T.B., Hebert T.E., Bernard D.J. Activins bind and signal via bone morphogenetic protein receptor type II (BMPR2) in immortalized gonadotrope-like cells. Cell Signal 2013, 25:2717-2726.
13. Bernabeu C., Lopez-Novoa J.M., Quintanilla M. The emerging role of TGF-beta superfamily coreceptors in cancer. Biochim Biophys Acta 2009, 1792:954-973.
14. Pietenpol J.A., Stein R.W., Moran E., Yaciuk P., Schlegel R., Lyons R.M., et al. TGF-beta 1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell 1990, 61:777-785.
15. Seoane J., Pouponnot C., Staller P., Schader M., Eilers M., Massague J. TGFbeta influences Myc, Miz-1 and Smad to control the CDK inhibitor p15INK4b. Nat Cell Biol 2001, 3:400-408.
16. Seoane J., Le H.V., Massague J. Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 2002, 419:729-734.
17. Kang Y., Chen C.R., Massague J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell 2003, 11:915-926.
18. Pardali K., Kowanetz M., Heldin C.H., Moustakas A. Smad pathway-specific transcriptional regulation of the cell cycle inhibitor p21(WAF1/Cip1). J Cell Physiol 2005, 204:260-272.
19. Sorrentino A., Thakur N., Grimsby S., Marcusson A., von Bulow V., Schuster N., et al. The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat Cell Biol 2008, 10:1199-1207.
20. Edlund S., Bu S., Schuster N., Aspenstrom P., Heuchel R., Heldin N.E., et al. Transforming growth factor-beta1 (TGF-beta)-induced apoptosis of prostate cancer cells involves Smad7-dependent activation of p38 by TGF-beta-activated kinase 1 and mitogen-activated protein kinase kinase 3. Mol Biol Cell 2003, 14:529-544.
21. Ramesh S., Qi X.J., Wildey G.M., Robinson J., Molkentin J., Letterio J., et al. TGF beta-mediated BIM expression and apoptosis are regulated through SMAD3-dependent expression of the MAPK phosphatase MKP2. EMBO Rep 2008, 9:990-997.
22. Spender L.C., O'Brien D.I., Simpson D., Dutt D., Gregory C.D., Allday M.J., et al. TGF-beta induces apoptosis in human B cells by transcriptional regulation of BIK and BCL-XL. Cell Death Differ 2009, 16:593-602.
23. Umulis D., O'Connor M.B., Blair S.S. The extracellular regulation of bone morphogenetic protein signaling. Development 2009, 136:3715-3728.
24. Avsian-Kretchmer O., Hsueh A.J. Comparative genomic analysis of the eight-membered ring cystine knot-containing bone morphogenetic protein antagonists. Mol Endocrinol 2004, 18:1-12.
25. Rosen V. BMP and BMP inhibitors in bone. Ann N Y Acad Sci 2006, 1068:19-25.
26. Kelley R., Ren R., Pi X., Wu Y., Moreno I., Willis M., et al. A concentration-dependent endocytic trap and sink mechanism converts Bmper from an activator to an inhibitor of Bmp signaling. J Cell Biol 2009, 184:597-609.
27. Itoh S., ten Dijke P. Negative regulation of TGF-beta receptor/Smad signal transduction. Curr Opin Cell Biol 2007, 19:176-184.
28. Norgaard N.N., Holien T., Jonsson S., Hella H., Espevik T., Sundan A., et al. CpG-oligodeoxynucleotide inhibits Smad-dependent bone morphogenetic protein signaling: effects on myeloma cell apoptosis and in vitro osteoblastogenesis. J Immunol 2010, 185:3131-3139.
29. Goto K., Kamiya Y., Imamura T., Miyazono K., Miyazawa K. Selective inhibitory effects of Smad6 on bone morphogenetic protein type I receptors. J Biol Chem 2007, 282:20603-20611.
30. Ro T.B., Holt R.U., Brenne A.T., Hjorth-Hansen H., Waage A., Hjertner O., et al. Bone morphogenetic protein-5, -6 and -7 inhibit growth and induce apoptosis in human myeloma cells. Oncogene 2004, 23:3024-3032.
31. Grcevic D., Kusec R., Kovacic N., Lukic A., Lukic I.K., Ivcevic S., et al. Bone morphogenetic proteins and receptors are over-expressed in bone-marrow cells of multiple myeloma patients and support myeloma cells by inducing ID genes. Leuk Res 2009, 34:742-751.
32. Hose D., Moreaux J., Meissner T., Seckinger A., Goldschmidt H., Benner A., et al. Induction of angiogenesis by normal and malignant plasma cells. Blood 2009, 114:128-143.
33. Seckinger A., Meissner T., Moreaux J., Goldschmidt H., Fuhler G.M., Benner A., et al. Bone morphogenic protein 6: a member of a novel class of prognostic factors expressed by normal and malignant plasma cells inhibiting proliferation and angiogenesis. Oncogene 2009, 28:3866-3879.
34. Lebrin F., Deckers M., Bertolino P., Ten Dijke P. TGF-beta receptor function in the endothelium. Cardiovasc Res 2005, 65:599-608.
35. Olsen O.E., Wader K.F., Misund K., Vatsveen T.K., Ro T.B., Mylin A.K., et al. Bone morphogenetic protein-9 suppresses growth of myeloma cells by signaling through ALK2 but is inhibited by endoglin. Blood Cancer J 2014, 4:e196.
36. Martinovic S., Mazic S., Kisic V., Basic N., Jakic-Razumovic J., Borovecki F., et al. Expression of bone morphogenetic proteins in stromal cells from human bone marrow long-term culture. J Histochem Cytochem 2004, 52:1159-1167.
37. Kersten C., Dosen G., Myklebust J.H., Sivertsen E.A., Hystad M.E., Smeland E.B., et al. BMP-6 inhibits human bone marrow B lymphopoiesis - upregulation of Id1 and Id3. Exp Hematol 2006, 34:72-81.
38. Maes K., Nemeth E., Roodman G.D., Huston A., Esteve F., Freytes C., et al. In anemia of multiple myeloma, hepcidin is induced by increased bone morphogenetic protein 2. Blood 2010, 116:3635-3644.
39. Baughn L.B., Di Liberto M., Niesvizky R., Cho H.J., Jayabalan D., Lane J., et al. CDK2 phosphorylation of Smad2 disrupts TGF-beta transcriptional regulation in resistant primary bone marrow myeloma cells. J Immunol 2009, 182:1810-1817.
40. Urashima M., Ogata A., Chauhan D., Hatziyanni M., Vidriales M.B., Dedera D.A., et al. Transforming growth factor-beta1: differential effects on multiple myeloma versus normal B cells. Blood 1996, 87:1928-1938.
41. Cook G., Campbell J.D., Carr C.E., Boyd K.S., Franklin I.M. Transforming growth factor beta from multiple myeloma cells inhibits proliferation and IL-2 responsiveness in T lymphocytes. J Leukoc Biol 1999, 66:981-988.
42. de Carvalho F., Colleoni G.W.B., Almeida M.S.S., Carvalho A.L., Vettore A.L. TGF beta R2 aberrant methylation is a potential prognostic marker and therapeutic target in multiple myeloma. Int J Cancer 2009, 125:1985-1991.
43. Lambert K.E., Huang H., Mythreye K., Blobe G.C. The type III transforming growth factor-beta receptor inhibits proliferation, migration, and adhesion in human myeloma cells. Mol Biol Cell 2011, 22:1463-1472.
44. Sanchez-Elsner T., Botella L.M., Velasco B., Langa C., Bernabeu C. Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. J Biol Chem 2002, 277:43799-43808.
45. Matsumoto T., Abe M. TGF-beta-related mechanisms of bone destruction in multiple myeloma. Bone 2011, 48:129-134.
46. Tsirakis G., Pappa C.A., Spanoudakis M., Chochlakis D., Alegakis A., Psarakis F.E., et al. Clinical significance of sCD105 in angiogenesis and disease activity in multiple myeloma. Eur J Intern Med 2012, 23:368-373.
47. Pappa C., Alexandrakis M., Boula A., Psarakis F., Kolovou A., Bantouna V., et al. Emerging roles of endoglin/CD105 and angiogenic cytokines for disease development and progression in multiple myeloma patients. Hematol Oncol 2013, 31:201-205.
48. Kawamura C., Kizaki M., Yamato K., Uchida H., Fukuchi Y., Hattori Y., et al. Bone morphogenetic protein-2 induces apoptosis in human myeloma cells with modulation of STAT3. Blood 2000, 96:2005-2011.
49. Hjertner O., Hjorth-Hansen H., Borset M., Seidel C., Waage A., Sundan A. Bone morphogenetic protein-4 inhibits proliferation and induces apoptosis of multiple myeloma cells. Blood 2001, 97:516-522.
50. Holien T., Vatsveen T.K., Hella H., Rampa C., Brede G., Groseth L.A., et al. Bone morphogenetic proteins induce apoptosis in multiple myeloma cells by Smad-dependent repression of MYC. Leukemia 2012, 26:1073-1080.
51. Kee B.L., Rivera R.R., Murre C. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-beta. Nat Immunol 2001, 2:242-247.
52. Sugai M., Gonda H., Kusunoki T., Katakai T., Yokota Y., Shimizu A. Essential role of Id2 in negative regulation of IgE class switching. Nat Immunol 2003, 4:25-30.
53. Kersten C., Sivertsen E.A., Hystad M.E., Forfang L., Smeland E.B., Myklebust J.H. BMP-6 inhibits growth of mature human B cells; induction of Smad phosphorylation and upregulation of Id1. BMC Immunol 2005, 6:9.
54. Kowanetz M., Valcourt U., Bergstrom R., Heldin C.H., Moustakas A. Id2 and Id3 define the potency of cell proliferation and differentiation responses to transforming growth factor beta and bone morphogenetic protein. Mol Cell Biol 2004, 24:4241-4254.
55. Fukuda N., Saitoh M., Kobayashi N., Miyazono K. Execution of BMP-4-induced apoptosis by p53-dependent ER dysfunction in myeloma and B-cell hybridoma cells. Oncogene 2006, 25:3509-3517.
56. Holien T., Vatsveen T.K., Hella H., Waage A., Sundan A. Addiction to c-MYC in multiple myeloma. Blood 2012, 120:2450-2453.
57. Holien T., Sundan A. Oncogene addiction to c-MYC in myeloma cells. Oncotarget 2012, 3:739-740.
58. Kassambara A., Hose D., Moreaux J., Reme T., Torrent J., Rossi J.F., et al. Identification of pluripotent and adult stem cell genes unrelated to cell cycle and associated with poor prognosis in multiple myeloma. PLoS ONE 2012, 7:e42161.
59. Katsuno Y., Hanyu A., Kanda H., Ishikawa Y., Akiyama F., Iwase T., et al. Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene 2008, 27:6322-6333.
60. Virk M.S., Petrigliano F.A., Liu N.Q., Chatziioannou A.F., Stout D., Kang C.O., et al. Influence of simultaneous targeting of the bone morphogenetic protein pathway and RANK/RANKL axis in osteolytic prostate cancer lesion in bone. Bone 2009, 44:160-167.
61. Kim S.J., Letterio J. Transforming growth factor-beta signaling in normal and malignant hematopoiesis. Leukemia 2003, 17:1731-1737.
62. Hayashi T., Hideshima T., Nguyen A.N., Munoz O., Podar K., Hamasaki M., et al. Transforming growth factor beta receptor I kinase inhibitor down-regulates cytokine secretion and multiple myeloma cell growth in the bone marrow microenvironment. Clin Cancer Res 2004, 10:7540-7546.
63. Fernandez T., Amoroso S., Sharpe S., Jones G.M., Bliskovski V., Kovalchuk A., et al. Disruption of transforming growth factor beta signaling by a novel ligand-dependent mechanism. J Exp Med 2002, 195:1247-1255.
64. Matsuura I., Denissova N.G., Wang G., He D., Long J., Liu F. Cyclin-dependent kinases regulate the antiproliferative function of Smads. Nature 2004, 430:226-231.
65. Nakano A., Koinuma D., Miyazawa K., Uchida T., Saitoh M., Kawabata M., et al. Pin1 down-regulates transforming growth factor-beta (TGF-beta) signaling by inducing degradation of Smad proteins. J Biol Chem 2009, 284:6109-6115.
66. Nishihara T., Okahashi N., Ueda N. Activin A induces apoptotic cell death. Biochem Biophys Res Commun 1993, 197:985-991.
67. Corre J., Mahtouk K., Attal M., Gadelorge M., Huynh A., Fleury-Cappellesso S., et al. Bone marrow mesenchymal stem cells are abnormal in multiple myeloma. Leukemia 2007, 21:1079-1088.
68. Tanno T., Lim Y., Wang Q., Chesi M., Bergsagel P.L., Matthews G., et al. Growth differentiating factor 15 enhances the tumor-initiating and self-renewal potential of multiple myeloma cells. Blood 2014, 123:725-733.
69. Shore E.M., Xu M., Feldman G.J., Fenstermacher D.A., Cho T.J., Choi I.H., et al. A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat Genet 2006, 38:525-527.
70. Seidel C., Borset M., Turesson I., Abildgaard N., Sundan A., Waage A. Elevated serum concentrations of hepatocyte growth factor in patients with multiple myeloma. The Nordic Myeloma Study Group. Blood 1998, 91:806-812.
71. Tian E., Zhan F., Walker R., Rasmussen E., Ma Y., Barlogie B., et al. The role of the Wnt-signaling antagonist DKK1 in the development of osteolytic lesions in multiple myeloma. N Engl J Med 2003, 349:2483-2494.
72. Standal T., Abildgaard N., Fagerli U.M., Stordal B., Hjertner O., Borset M., et al. HGF inhibits BMP-induced osteoblastogenesis: possible implications for the bone disease of multiple myeloma. Blood 2007, 109:3024-3030.
73. Tsai S.Y., Huang Y.L., Yang W.H., Tang C.H. Hepatocyte growth factor-induced BMP-2 expression is mediated by c-Met receptor, FAK, JNK, Runx2, and p300 pathways in human osteoblasts. Int Immunopharmacol 2012, 13:156-162.
74. Qiang Y.W., Barlogie B., Rudikoff S., Shaughnessy J.D. Dkk1-induced inhibition of Wnt signaling in osteoblast differentiation is an underlying mechanism of bone loss in multiple myeloma. Bone 2008, 42:669-680.
75. Krause C., Korchynskyi O., de Rooij K., Weidauer S.E., de Gorter D.J., van Bezooijen R.L., et al. Distinct modes of inhibition by sclerostin on bone morphogenetic protein and Wnt signaling pathways. J Biol Chem 2010, 285:41614-41626.
76. Colucci S., Brunetti G., Oranger A., Mori G., Sardone F., Specchia G., et al. Myeloma cells suppress osteoblasts through sclerostin secretion. Blood Cancer J 2011, 1:e27.
77. Terpos E., Christoulas D., Gkotzamanidou M., Bratengeier C., Gavriatopoulou M., Migkou M., et al. Circulating levels of the Wnt inhibitors Dickkopf-1 and sclerostin in different phases of multiple myeloma: alterations post-therapy with lenalidomide and dexamethasone with or without bortezomib. Blood 2010, 116. abstr. 2963.
78. Oshima T., Abe M., Asano J., Hara T., Kitazoe K., Sekimoto E., et al. Myeloma cells suppress bone formation by secreting a soluble Wnt inhibitor, sFRP-2. Blood 2005, 106:3160-3165.
79. Ehrlich L.A., Chung H.Y., Ghobrial I., Choi S.J., Morandi F., Colla S., et al. IL-3 is a potential inhibitor of osteoblast differentiation in multiple myeloma. Blood 2005, 106:1407-1414.
80. Silbermann R., Bolzoni M., Storti P., Guasco D., Bonomini S., Zhou D., et al. Bone marrow monocyte-/macrophage-derived activin A mediates the osteoclastogenic effect of IL-3 in multiple myeloma. Leukemia 2014, 28:951-954.
81. Vallet S., Mukherjee S., Vaghela N., Hideshima T., Fulciniti M., Pozzi S., et al. Activin A promotes multiple myeloma-induced osteolysis and is a promising target for myeloma bone disease. Proc Natl Acad Sci U S A 2010, 107:5124-5129.
82. Chantry A.D., Heath D., Mulivor A.W., Pearsall S., Baud'huin M., Coulton L., et al. Inhibiting activin-A signaling stimulates bone formation and prevents cancer-induced bone destruction in vivo. J Bone Miner Res 2010, 25:2633-2646.
83. Scullen T., Santo L., Vallet S., Fulciniti M., Eda H., Cirstea D., et al. Lenalidomide in combination with an activin A-neutralizing antibody: preclinical rationale for a novel anti-myeloma strategy. Leukemia 2013, 27:1715-1721.
84. Ganz T. Hepcidin and iron regulation, 10 years later. Blood 2011, 117:4425-4433.
85. Nauth A., Ristevski B., Li R., Schemitsch E.H. Growth factors and bone regeneration: how much bone can we expect. Injury 2011, 42:574-579.
86. Shah R.K., Moncayo V.M., Smitson R.D., Pierre-Jerome C., Terk M.R. Recombinant human bone morphogenetic protein 2-induced heterotopic ossification of the retroperitoneum, psoas muscle, pelvis and abdominal wall following lumbar spinal fusion. Skeletal Radiol 2010, 39:501-504.
87. Hughes A.P., Taher F., Farshad M., Aichmair A. Multiple myeloma exacerbation following utilization of bone morphogenetic protein-2 in lateral lumbar interbody fusion: a case report and review of the literature. Spine J 2014, 14:e13-e19.
88. Epstein N.E. Complications due to the use of BMP/INFUSE in spine surgery: the evidence continues to mount. Surg Neurol Int 2013, 4:S343-S352.
89. Abdulkadyrov K., Salogub G., Khuazheva N., Woolf R., Haltorn E., Borgstein N., et al. ACE-011, a soluble activin receptor type Iia IgG-Fc fusion protein, increases hemoglobin (Hb) and improves bone lesions in multiple myeloma patients receiving myelosuppressive chemotherapy: preliminary analysis. Blood 2009, 114. abstr 749.
90. Maguer-Satta V., Bartholin L., Jeanpierre S., Ffrench M., Martel S., Magaud J.P., et al. Regulation of human erythropoiesis by activin A, BMP2, and BMP4, members of the TGFbeta family. Exp Cell Res 2003, 282:110-120.
91. Fields S.Z., Parshad S., Anne M., Raftopoulos H., Alexander M.J., Sherman M.L., et al. Activin receptor antagonists for cancer-related anemia and bone disease. Expert Opin Investig Drugs 2013, 22:87-101.
92. Abdulkadyrov K.M., Salogub G.N., Khuazheva N.K., Sherman M.L., Laadem A., Barger R., et al. Sotatercept in patients with osteolytic lesions of multiple myeloma. Br J Haematol 2014, [Epub ahead of print].
93. Bendell J.C., Gordon M.S., Hurwitz H.I., Jones S.F., Mendelson D.S., Blobe G.C., et al. Safety, pharmacokinetics, pharmacodynamics, and antitumor activity of dalantercept, an activin receptor-like kinase-1 ligand trap, in patients with advanced cancer. Clin Cancer Res 2014, 20:480-489.
94. David L., Mallet C., Mazerbourg S., Feige J.J., Bailly S. Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 2007, 109:1953-1961.
95. Baud'huin M., Solban N., Cornwall-Brady M., Sako D., Kawamoto Y., Liharska K., et al. A soluble bone morphogenetic protein type IA receptor increases bone mass and bone strength. Proc Natl Acad Sci U S A 2012, 109:12207-12212.
96. van Meeteren L.A., Thorikay M., Bergqvist S., Pardali E., Stampino C.G., Hu-Lowe D., et al. Anti-human activin receptor-like kinase 1 (ALK1) antibody attenuates bone morphogenetic protein 9 (BMP9)-induced ALK1 signaling and interferes with endothelial cell sprouting. J Biol Chem 2012, 287:18551-18561.
97. Yu P.B., Hong C.C., Sachidanandan C., Babitt J.L., Deng D.Y., Hoyng S.A., et al. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 2008, 4:33-41.
98. Boergermann J.H., Kopf J., Yu P.B., Knaus P. Dorsomorphin and LDN-193189 inhibit BMP-mediated Smad, p38 and Akt signalling in C2C12 cells. Int J Biochem Cell Biol 2010, 42:1802-1807.
99. Hao J., Ho J.N., Lewis J.A., Karim K.A., Daniels R.N., Gentry P.R., et al. In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem Biol 2010, 5:245-253.
100. Mohedas A.H., Xing X., Armstrong K.A., Bullock A.N., Cuny G.D., Yu P.B. Development of an ALK2-biased BMP type I receptor kinase inhibitor. ACS Chem Biol 2013, 8:1291-1302.