Bone morphogenetic protein-9 suppresses growth of myeloma cells by signaling through ALK2 but is inhibited by endoglin

Blood Cancer Journal

Volumn 4, Issue 3, 2014, Pages

  Olsen, O E ^a   Wader, K F ^a,b   Misund, K ^a   Vatsveen T K ^a   Ro T B ^a,b   Mylin, A K ^c   Turesson, I ^d   Stordal B F ^a   Moen, S H ^a   Standal, T ^a   Waage, A ^a,b   Sundan, A ^a   Holien, T ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN 9; BONE MORPHOGENETIC PROTEIN RECEPTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; ENDOGLIN; PROTEIN ALK 2; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BONE MARROW; CANCER GROWTH; CANCER INHIBITION; CANCER PATIENT; CANCER SURVIVAL; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; MICROENVIRONMENT; MULTIPLE MYELOMA CELL LINE; MYELOMA CELL; ONCOGENE C MYC; OVERALL SURVIVAL; PRIMARY CELL; PROGRESSION FREE SURVIVAL; PROTEIN BLOOD LEVEL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84901840766     PISSN: None     EISSN: 20445385     Source Type: Journal    
DOI: 10.1038/bcj.2014.16     Document Type: Article

References (46)

1. Mahindra A, Laubach J, Raje N, Munshi N, Richardson PG, Anderson K. Latest advances and current challenges in the treatment of multiple myeloma. Nat Rev Clin Oncol 2012; 9: 135-143.
2. 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.
3. 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.
4. Ro TB, Holt RU, Brenne AT, 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.
5. Holien T, Vatsveen TK, Hella H, Rampa C, Brede G, Groseth LA et al. Bone morphogenetic proteins induce apoptosis in multiple myeloma cells by Smaddependent repression of MYC. Leukemia 2012; 26: 1073-1080.
6. Seckinger A, Meissner T, Moreaux J, Goldschmidt H, Fuhler GM, 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.
7. Vukicevic S, Grgurevic L. BMP-6 and mesenchymal stem cell differentiation. Cytokine Growth Factor Rev 2009; 20: 441-448.
8. Cheng H, Jiang W, Phillips FM, Haydon RC, Peng Y, Zhou L et al. Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs). J Bone Joint Surg Am 2003; 85-A: 1544-1552.
9. Kang Q, Sun MH, Cheng H, Peng Y, Montag AG, Deyrup AT et al. Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adenovirus-mediated gene delivery. Gene Ther 2004; 11: 1312-1320.
10. Fong D, Bisson M, Laberge G, McManus S, Grenier G, Faucheux N et al. Bone morphogenetic protein-9 activates Smad and ERK pathways and supports human osteoclast function and survival in vitro. Cell Signal 2013; 25: 717-728.
11. David L, Mallet C, Keramidas M, Lamande N, Gasc JM, Dupuis-Girod S et al. Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ Res 2008; 102: 914-922.
12. Herrera B, Inman GJ. 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 2009; 10: 20.
13. Bidart M, Ricard N, Levet S, Samson M, Mallet C, David L et al. BMP9 is produced by hepatocytes and circulates mainly in an active mature form complexed to its prodomain. Cell Mol Life Sci 2012; 69: 313-324.
14. Suttapreyasri S, Koontongkaew S, Phongdara A, Leggat U. Expression of bone morphogenetic proteins in normal human intramembranous and endochondral bones. Int J Oral Maxillofac Surg 2006; 35: 444-452.
15. Bragdon B, Moseychuk O, Saldanha S, King D, Julian J, Nohe A. Bone morphogenetic proteins: a critical review. Cell Signal 2011; 23: 609-620.
16. David L, Mallet C, Mazerbourg S, Feige JJ, 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.
17. Herrera B, van Dinther M, Ten Dijke P, Inman GJ. Autocrine bone morphogenetic protein-9 signals through activin receptor-like kinase-2/Smad1/Smad4 to promote ovarian cancer cell proliferation. Cancer Res 2009; 69: 9254-9262.
18. 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.
19. Ye L, Kynaston H, Jiang WG. Bone morphogenetic protein-9 induces apoptosis in prostate cancer cells, the role of prostate apoptosis response-4. Mol Cancer Res 2008; 6: 1594-1606.
20. Ye L, Kynaston H, Jiang WG. Bone morphogenetic protein-10 suppresses the growth and aggressiveness of prostate cancer cells through a Smad independent pathway. J Urol 2009; 181: 2749-2759.
21. Wang K, Feng H, Ren W, Sun X, Luo J, Tang M et al. BMP9 inhibits the proliferation and invasiveness of breast cancer cells MDA-MB-231. J Cancer Res Clin Oncol 2011; 137: 1687-1696.
22. Ye L, Bokobza S, Li J, Moazzam M, Chen J, Mansel RE et al. Bone morphogenetic protein-10 (BMP-10) inhibits aggressiveness of breast cancer cells and correlates with poor prognosis in breast cancer. Cancer Sci 2010; 101: 2137-2144.
23. Herrera B, Garcia-Alvaro M, Cruz S, Walsh P, Fernandez M, Roncero C et al. BMP9 is a proliferative and survival factor for human hepatocellular carcinoma cells. PLoS One 2013; 8: e69535.
24. Castonguay R, Werner ED, Matthews RG, Presman E, Mulivor AW, Solban N et al. Soluble endoglin specifically binds bone morphogenetic proteins 9 and 10 via its orphan domain, inhibits blood vessel formation, and suppresses tumor growth. J Biol Chem 2011; 286: 30034-30046.
25. Scharpfenecker M, van Dinther M, Liu Z, van Bezooijen RL, Zhao Q, Pukac L et al. BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J Cell Sci 2007; 120: 964-972.
26. Barbara NP, Wrana JL, Letarte M. Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-beta superfamily. J Biol Chem 1999; 274: 584-594.
27. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M et al. Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 2004; 23: 4018-4028.
28. Jonker L, Arthur HM. Endoglin expression in early development is associated with vasculogenesis and angiogenesis. Mech Dev 2002; 110: 193-196.
29. Pruneri G, Ponzoni M, Ferreri AJ, Decarli N, Tresoldi M, Raggi F et al. Microvessel density, a surrogate marker of angiogenesis, is significantly related to survival in multiple myeloma patients. Br J Haematol 2002; 118: 817-820.
30. Duff SE, Li C, Garland JM, Kumar S. CD105 is important for angiogenesis: evidence and potential applications. FASEB J 2003; 17: 984-992.
31. Wang JM, Wilson PB, Kumar S, Pye D, Hunter RD. Quantitation of endothelial cell specific protein E-9 employing a single monoclonal antibody in an indirect sandwich ELISA. J Immunol Methods 1994; 171: 55-64.
32. Li C, Guo B, Wilson PB, Stewart A, Byrne G, Bundred N et al. Plasma levels of soluble CD105 correlate with metastasis in patients with breast cancer. Int J Cancer 2000; 89: 122-126.
33. Calabro L, Fonsatti E, Bellomo G, Alonci A, Colizzi F, Sigalotti L et al. Differential levels of soluble endoglin (CD105) in myeloid malignancies. J Cell Physiol 2003; 194: 171-175.
34. Tsirakis G, Pappa CA, Spanoudakis M, Chochlakis D, Alegakis A, Psarakis FE et al. Clinical significance of sCD105 in angiogenesis and disease activity in multiple myeloma. Eur J Intern Med 2012; 23: 368-373.
35. 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; 34: 201-205.
36. Misund K, Baranowska KA, Holien T, Rampa C, Klein DC, Borset M et al. A method for measurement of drug sensitivity of myeloma cells co-cultured with bone marrow stromal cells. J Biomol Screen 2013; 18: 637-646.
37. Vindelov LL, Christensen IJ, Nissen NI. A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 1983; 3: 323-327.
38. Holien T, Olsen OE, Misund K, Hella H, Waage A, Ro TB et al. Lymphoma and myeloma cells are highly sensitive to growth arrest and apoptosis induced by artesunate. Eur J Haematol 2013; 91: 339-346.
39. Fagerli UM, Holt RU, Holien T, Vaatsveen TK, Zhan F, Egeberg KW et al. Overexpression and involvement in migration by the metastasis-associated phosphatase PRL-3 in human myeloma cells. Blood 2008; 111: 806-815.
40. Gimsing P, Carlson K, Turesson I, Fayers P, Waage A, Vangsted A et al. Effect of pamidronate 30 mg versus 90 mg on physical function in patients with newly diagnosed multiple myeloma (Nordic Myeloma Study Group): a double-blind, randomised controlled trial. Lancet Oncol 2010; 11: 973-982.
41. Wader KF, Fagerli UM, Holt RU, Stordal B, Borset M, Sundan A et al. Elevated serum concentrations of activated hepatocyte growth factor activator in patients with multiple myeloma. Eur J Haematol 2008; 81: 380-383.
42. Holien T, Vatsveen TK, Hella H, Waage A, Sundan A. Addiction to c-MYC in multiple myeloma. Blood 2012; 120: 2450-2453.
43. Hao J, Ho JN, Lewis JA, Karim KA, Daniels RN, Gentry PR et al. In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem Biol 2010; 5: 245-253.
44. Korchynskyi O, ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 2002; 277: 4883-4891.
45. Baughn LB, Di Liberto M, Niesvizky R, Cho HJ, 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.
46. Huse K, Bakkebo M, Walchli S, Oksvold MP, Hilden VI, Forfang L et al. Role of Smad proteins in resistance to BMP-induced growth inhibition in B-cell lymphoma. PLoS One 2012; 7: e46117.