Bone morphogenetic protein modulator BMPER is highly expressed in malignant tumors and controls invasive cell behavior

Oncogene

Volumn 31, Issue 24, 2012, Pages 2919-2930

  Heinke, J ^a   Kerber, M ^a   Rahner, S ^a   Mnich, L ^a   Lassmann, S ^b   Helbing, T ^a   Werner, M ^b   Patterson, C ^c   Bode, C ^a   Moser, M ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

BMPER; BMPs; MMPs; tumor angiogenesis; tumor progression

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN ENDOTHELIAL CELL PRECURSOR DERIVED REGULATOR; DNA BINDING PROTEIN; GELATINASE A; GELATINASE B; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; C57BL 6 MOUSE; CANCER CELL; CANCER CELL CULTURE; CANCER INVASION; CANCER MODEL; CANCER TRANSPLANTATION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; COLON CARCINOMA; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LEWIS CARCINOMA; LUNG CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; UTERINE CERVIX CARCINOMA;

ANIMALS; CARCINOMA, LEWIS LUNG; CARRIER PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; COLONIC NEOPLASMS; FEMALE; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; UTERINE CERVICAL NEOPLASMS;

MUS;

EID: 84862314825     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.473     Document Type: Article

References (70)

1. Alarmo EL, Kallioniemi A. (2010). Bone morphogenetic proteins in breast cancer: dual role in tumourigenesis? Endocr Relat Cancer 17: R123-R139.
2. Arihiro K, Inai K. (2001). Expression of CD31, Met/hepatocyte growth factor receptor and bone morphogenetic protein in bone metastasis of osteosarcoma. Pathol Int 51: 100-106. (Pubitemid 32174735)
3. Bailey JM, Singh PK, Hollingsworth MA. (2007). Cancer metastasis facilitated by developmental pathways: Sonic hedgehog, Notch, and bone morphogenic proteins. J Cell Biochem 102: 829-839. (Pubitemid 350036923)
4. Balemans W, Van Hul W. (2002). Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev Biol 250: 231-250. (Pubitemid 35216412)
5. Balmanno K, Cook SJ. (2009). Tumour cell survival signalling by the ERK1/2 pathway. Cell Death Differ 16: 368-377.
6. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K et al. (2000). Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2: 737-744.
7. Blish KR, Wang W, Willingham MC, Du W, Birse CE, Krishnan SR et al. (2008). A human bone morphogenetic protein antagonist is down-regulated in renal cancer. Mol Biol Cell 19: 457-464. (Pubitemid 351272135)
8. Brunkow ME, Gardner JC, Van Ness J, Paeper BW, Kovacevich BR, Proll S et al. (2001). Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am J Hum Genet 68: 577-589. (Pubitemid 32202753)
9. Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, Que I, Schwaninger R et al. (2007a). Bone morphogenetic protein 7 in the development and treatment of bone metastases from breast cancer. Cancer Res 67: 8742-8751. (Pubitemid 47437450)
10. Buijs JT, Rentsch CA, van der Horst G, van Overveld PG, Wetterwald A, Schwaninger R et al. (2007b). BMP7, a putative regulator of epithelial homeostasis in the human prostate, is a potent inhibitor of prostate cancer bone metastasis in vivo. Am J Pathol 171: 1047-1057. (Pubitemid 47441001)
11. Conley CA, Silburn R, Singer MA, Ralston A, Rohwer-Nutter D, Olson DJ et al. (2000). Crossveinless 2 contains cysteine-rich domains and is required for high levels of BMP-like activity during the formation of the cross veins in Drosophila. Development 127: 3947-3959.
12. Deckers MM, van Bezooijen RL, van der Horst G, Hoogendam J, van Der Bent C, Papapoulos SE et al. (2002). Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology 143: 1545-1553. (Pubitemid 34274386)
13. Deng H, Makizumi R, Ravikumar TS, Dong H, Yang W, Yang WL. (2007). Bone morphogenetic protein-4 is overexpressed in colonic adenocarcinomas and promotes migration and invasion of HCT116 cells. Exp Cell Res 313: 1033-1044. (Pubitemid 46273448)
14. Doki Y, Murakami K, Yamaura T, Sugiyama S, Misaki T, Saiki I. (1999). Mediastinal lymph node metastasis model by orthotopic intrapulmonary implantation of Lewis lung carcinoma cells in mice. Br J Cancer 79: 1121-1126. (Pubitemid 29087884)
15. Egeblad M, Werb Z. (2002). New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2: 161-174. (Pubitemid 37328786)
16. Feeley BT, Gamradt SC, Hsu WK, Liu N, Krenek L, Robbins P et al. (2005). Influence of BMPs on the formation of osteoblastic lesions in metastatic prostate cancer. J Bone Miner Res 20: 2189-2199. (Pubitemid 41698782)
17. Fidler IJ. (2003). The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 3: 453-458.
18. Gautschi O, Tepper CG, Purnell PR, Izumiya Y, Evans CP, Green TP et al. (2008). Regulation of Id1 expression by SRC: implications for targeting of the bone morphogenetic protein pathway in cancer. Cancer Res 68: 2250-2258. (Pubitemid 351521798)
19. Gordon KJ, Kirkbride KC, How T, Blobe GC. (2009). Bone Morphogenetic Proteins Induce Pancreatic Cancer Cell Invasiveness through a Smad1-dependent Mechanism that Involves Matrix Metalloproteinase Protein-2. Carcinogenesis 30: 238-248.
20. Goumans MJ, Liu Z, ten Dijke P. (2009). TGF-beta signaling in vascular biology and dysfunction. Cell Res 19: 116-127.
21. Hanahan D, Weinberg RA. (2011). Hallmarks of cancer: the next generation. Cell 144: 646-674.
22. Heinke J, Wehofsits L, Zhou Q, Zoeller C, Baar KM, Helbing T et al. (2008). BMPER is an endothelial cell regulator and controls bone morphogenetic protein-4-dependent angiogenesis. Circ Res 103: 804-812.
23. Huang SC, Sheu BC, Chang WC, Cheng CY, Wang PH, Lin S. (2009). Extracellular matrix proteases - cytokine regulation role in cancer and pregnancy. Front Biosci 14: 1571-1588.
24. Iemura S, Yamamoto TS, Takagi C, Uchiyama H, Natsume T, Shimasaki S et al. (1998). Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo. Proc Natl Acad Sci USA 95: 9337-9342. (Pubitemid 28506232)
25. Ikeya M, Kawada M, Kiyonari H, Sasai N, Nakao K, Furuta Y et al. (2006). Essential pro-Bmp roles of crossveinless 2 in mouse organogenesis. Development 133: 4463-4473. (Pubitemid 46017821)
26. Katsuno Y, Hanyu A, Kanda H, Ishikawa Y, Akiyama F, Iwase T et al. (2008). Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene 27: 6322-6333.
27. Kelley R, Ren R, Pi X, Wu Y, Moreno I, Willis M et al. (2009). A concentration-dependent endocytic trap and sink mechanism converts Bmper from an activator to an inhibitor of Bmp signaling. J Cell Biol 184: 597-609.
28. Klose A, Waerzeggers Y, Monfared P, Vukicevic S, Kaijzel EL, Winkeler A et al. (2011). Imaging bone morphogenetic protein 7 induced cell cycle arrest in experimental gliomas. Neoplasia 13: 276-285.
29. Krause C, Korchynskyi O, de Rooij K, Weidauer SE, de Gorter DJ, van Bezooijen RL et al. (2010). Distinct modes of inhibition by sclerostin on bone morphogenetic protein and Wnt signaling pathways. J Biol Chem 285: 41614-41626.
30. Langenfeld EM, Calvano SE, Abou-Nukta F, Lowry SF, Amenta P, Langenfeld J. (2003). The mature bone morphogenetic protein-2 is aberrantly expressed in non-small cell lung carcinomas and stimulates tumor growth of A549 cells. Carcinogenesis 24: 1445-1454. (Pubitemid 37160834)
31. Langenfeld EM, Kong Y, Langenfeld J. (2006). Bone morphogenetic protein 2 stimulation of tumor growth involves the activation of Smad-1/5. Oncogene 25: 685-692. (Pubitemid 43214695)
32. Langenfeld EM, Langenfeld J. (2004). Bone morphogenetic protein-2 stimulates angiogenesis in developing tumors. Mol Cancer Res 2: 141-149. (Pubitemid 39030304)
33. Laurikkala J, Kassai Y, Pakkasjarvi L, Thesleff I, Itoh N. (2003). Identification of a secreted BMP antagonist, ectodin, integrating BMP, FGF, and SHH signals from the tooth enamel knot. Dev Biol 264: 91-105. (Pubitemid 37393449)
34. Lin KY, Lu D, Hung CF, Peng S, Huang L, Jie C et al. (2007). Ectopic expression of vascular cell adhesion molecule-1 as a new mechanism for tumor immune evasion. Cancer Res 67: 1832-1841. (Pubitemid 46383410)
35. Ling MT, Lau TC, Zhou C, Chua CW, Kwok WK, Wang Q et al. (2005). Overexpression of Id-1 in prostate cancer cells promotes angiogenesis through the activation of vascular endothelial growth factor (VEGF). Carcinogenesis 26: 1668-1676. (Pubitemid 41487982)
36. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R et al. (1999). Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401: 670-677.
37. Maegdefrau U, Amann T, Winklmeier A, Braig S, Schubert T, Weiss TS et al. (2009). Bone morphogenetic protein 4 is induced in hepatocellular carcinoma by hypoxia and promotes tumour progression. J Pathol 218: 520-529.
38. Miyazono K, Miyazawa K. (2002). Id: a target of BMP signaling. Sci STKE 2002: pe40.
39. Moll F, Millet C, Noel D, Orsetti B, Bardin A, Katsaros D et al. (2006). Chordin is underexpressed in ovarian tumors and reduces tumor cell motility. FASEB J 20: 240-250. (Pubitemid 44933171)
40. Moser M, Binder O, Wu Y, Aitsebaomo J, Ren R, Bode C et al. (2003). BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol Cell Biol 23: 5664-5679. (Pubitemid 36951331)
41. Moser M, Patterson C. (2005). Bone morphogenetic proteins and vascular differentiation: BMPing up vasculogenesis. Thromb Haemost 94: 713-718. (Pubitemid 41489229)
42. Oelgeschlager M, Larrain J, Geissert D, De Robertis EM. (2000). The evolutionarily conserved BMP-binding protein twisted gastrulation promotes BMP signalling. Nature 405: 757-763. (Pubitemid 30407840)
43. Orlichenko LS, Radisky DC. (2008). Matrix metalloproteinases stimulate epithelial-mesenchymal transition during tumor development. Clin Exp Metastasis 25: 593-600.
44. Piccolo S, Agius E, Leyns L, Bhattacharyya S, Grunz H, Bouwmeester T et al. (1999). The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397: 707-710.
45. Piccolo S, Sasai Y, Lu B, De Robertis EM. (1996). Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86: 589-598. (Pubitemid 26299490)
46. Pouliot F, Labrie C. (2002). Role of Smad1 and Smad4 proteins in the induction of p21WAF1,Cip1 during bone morphogenetic protein-induced growth arrest in human breast cancer cells. J Endocrinol 172: 187-198. (Pubitemid 34082957)
47. Raida M, Clement JH, Ameri K, Han C, Leek RD, Harris AL. (2005). Expression of bone morphogenetic protein 2 in breast cancer cells inhibits hypoxic cell death. Int J Oncol 26: 1465-1470.
48. Rentzsch F, Zhang J, Kramer C, Sebald W, Hammerschmidt M. (2006). Crossveinless 2 is an essential positive feedback regulator of Bmp signaling during zebrafish gastrulation. Development 133: 801-811.
49. Rothhammer T, Bataille F, Spruss T, Eissner G, Bosserhoff AK. (2007). Functional implication of BMP4 expression on angiogenesis in malignant melanoma. Oncogene 26: 4158-4170. (Pubitemid 46920167)
50. Rothhammer T, Braig S, Bosserhoff AK. (2008). Bone morphogenetic proteins induce expression of metalloproteinases in melanoma cells and fibroblasts. Eur J Cancer 44: 2526-2534.
51. Rothhammer T, Poser I, Soncin F, Bataille F, Moser M, Bosserhoff AK. (2005). Bone morphogenic proteins are overexpressed in malignant melanoma and promote cell invasion and migration. Cancer Res 65: 448-456.
52. Schmierer B, Hill CS. (2007). TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8: 970-982. (Pubitemid 350174642)
53. Serpe M, Umulis D, Ralston A, Chen J, Olson DJ, Avanesov A et al. (2008). The BMP-binding protein Crossveinless 2 is a short-range, concentration- dependent, biphasic modulator of BMP signaling in Drosophila. Dev Cell 14: 940-953. (Pubitemid 351757202)
54. Smith WC, Harland RM. (1992). Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70: 829-840.
55. Soda H, Raymond E, Sharma S, Lawrence R, Cerna C, Gomez L et al. (1998). Antiproliferative effects of recombinant human bone morphogenetic protein-2 on human tumor colony-forming units. Anticancer Drugs 9: 327-331. (Pubitemid 28241822)
56. Stabile H, Mitola S, Moroni E, Belleri M, Nicoli S, Coltrini D et al. (2007). Bone morphogenic protein antagonist Drm/gremlin is a novel proangiogenic factor. Blood 109: 1834-1840. (Pubitemid 46348177)
57. ten Dijke P, Korchynskyi O, Valdimarsdottir G, Goumans MJ. (2003). Controlling cell fate by bone morphogenetic protein receptors. Mol Cell Endocrinol 211: 105-113. (Pubitemid 37491242)
58. Thawani JP, Wang AC, Than KD, Lin CY, La Marca F, Park P. (2010). Bone morphogenetic proteins and cancer: review of the literature. Neurosurgery 66: 233-246, discussion 246.
59. Thiery JP, Sleeman JP. (2006). Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142. (Pubitemid 43278296)
60. Umulis D, O'Connor MB, Blair SS. (2009). The extracellular regulation of bone morphogenetic protein signaling. Development 136: 3715-3728.
61. Valdimarsdottir G, Goumans MJ, Rosendahl A, Brugman M, Itoh S, Lebrin F et al. (2002). Stimulation of Id1 expression by bone morphogenetic protein is sufficient and necessary for bone morphogenetic protein-induced activation of endothelial cells. Circulation 106: 2263-2270. (Pubitemid 35222223)
62. Weiss KR, Cooper GM, Jadlowiec JA, McGough III RL, Huard J. (2006). VEGF and BMP expression in mouse osteosarcoma cells. Clin Orthop Relat Res 450: 111-117. (Pubitemid 44342124)
63. Wong ML, Medrano JF. (2005). Real-time PCR for mRNA quantitation. Biotechniques 39: 75-85.
64. Wu JB, Fu HQ, Huang LZ, Liu AW, Zhang JX. (2011). Effects of siRNA-targeting BMP-2 on the abilities of migration and invasion of human liver cancer SMMC7721 cells and its mechanism. Cancer Gene Ther 18: 20-25.
65. Yamashita H, ten Dijke P, Huylebroeck D, Sampath TK, Andries M, Smith JC et al. (1995). Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J Cell Biol 130: 217-226.
66. Yanagita M, Oka M, Watabe T, Iguchi H, Niida A, Takahashi S et al. (2004). USAG-1: a bone morphogenetic protein antagonist abundantly expressed in the kidney. Biochem Biophys Res Commun 316: 490-500. (Pubitemid 38338618)
67. Yang S, Zhong C, Frenkel B, Reddi AH, Roy-Burman P. (2005). Diverse biological effect and Smad signaling of bone morphogenetic protein 7 in prostate tumor cells. Cancer Res 65: 5769-5777. (Pubitemid 40911180)
68. Yu X, He F, Zhang T, Espinoza-Lewis RA, Lin L, Yang J et al. (2008). Cerberus functions as a BMP agonist to synergistically induce nodal expression during left-right axis determination in the chick embryo. Dev Dyn 237: 3613-3623.
69. Zhao H, Ayrault O, Zindy F, Kim JH, Roussel MF. (2008). Post-transcriptional down-regulation of Atoh1/Math1 by bone morphogenic proteins suppresses medulloblastoma development. Genes Dev 22: 722-727. (Pubitemid 351439102)
70. Zhou Q, Heinke J, Vargas A, Winnik S, Krauss T, Bode C et al. (2007). ERK signaling is a central regulator for BMP-4 dependent capillary sprouting. Cardiovasc Res 76: 390-399. (Pubitemid 350007461)