Bone morphogenetic protein 4 (BMP4) is required for migration and invasion of breast cancer

Molecular and Cellular Biochemistry

Volumn 363, Issue 1-2, 2012, Pages 179-190

  Guo, Dan ^a   Huang, Jiayi ^a   Gong, Jianping ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

BMP4; Breast cancer; CXCR4; Metastases; MMP 1

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CHEMOKINE RECEPTOR CXCR4; INTERSTITIAL COLLAGENASE; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INVASION; HUMAN; HUMAN CELL; METASTASIS; PROTEIN EXPRESSION;

ACTIVIN RECEPTORS; BONE MORPHOGENETIC PROTEIN 4; BREAST NEOPLASMS; CARRIER PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; COCULTURE TECHNIQUES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; MATRIX METALLOPROTEINASE 1; NEOPLASM INVASIVENESS; OSTEOBLASTS; OSTEOPROTEGERIN; PHENOTYPE; RANK LIGAND; RECEPTORS, CXCR4; RNA INTERFERENCE; RNA, MESSENGER; SMAD PROTEINS; TIME FACTORS; TRANSFECTION;

EID: 84857896322     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-011-1170-1     Document Type: Article

References (56)

1. Plunkett TA, Smith P, Rubens RD (2000) Risk of complications from bone metastases in breast cancer - implications for management. Eur J Cancer 36:476-482 (Pubitemid 30136225)
2. Wozney JM (2002) Overview of bone morphogenetic proteins. Spine (Phila Pa 1976) 27:S2-S8
3. Hogan BL (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 10:1580-1594
4. Alarmo E-L, Kuukasjärvi T, Karhu R, Kallioniemi A (2006) A comprehensive expression survey of bone morphogenetic proteins in breast cancer highlights the importance of BMP4 and BMP7. Breast Cancer Res Treat 103:239-246. doi:10.1007/s10549-006-9362-1 (Pubitemid 46789146)
5. Katsuno Y, Hanyu A, Kanda H, Ishikawa Y, Akiyama F, Iwase T, Ogata E, Ehata S, Miyazono K, Imamura T (2008) Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene 27:6322-6333. doi:10.1038/onc.2008.232
6. Helms MW, Packeisen J, August C, Schittek B, Boecker W, Brandt BH, Buerger H (2005) First evidence supporting a potential role for the BMP/SMAD pathway in the progression of oestrogen receptor-positive breast cancer. J Pathol 206:366-376. doi:10.1002/path.1785 (Pubitemid 40903201)
7. Clement JH, Raida M, Sanger J, Bicknell R, Liu J, Naumann A, Geyer A, Waldau A, Hortschansky P, Schmidt A, Hoffken K, Wolft S, Harris AL (2005) Bone morphogenetic protein 2 (BMP-2) induces in vitro invasion and in vivo hormone independent growth of breast carcinoma cells. Int J Oncol 27:401-407
8. Raida M, Clement JH, Leek RD, Ameri K, Bicknell R, Niederwieser D, Harris AL (2005) Bone morphogenetic protein 2 (BMP-2) and induction of tumor angiogenesis. J Cancer Res Clin Oncol 131:741-750. doi:10.1007/s00432-005-0024-1 (Pubitemid 41577951)
9. Du J, Yang S, An D, Hu F, Yuan W, Zhai C, Zhu T (2009) BMP-6 inhibits microRNA-21 expression in breast cancer through repressing deltaEF1 and AP-1. Cell Res 19:487-496. doi:10.1038/cr.2009.34
10. Yang S, Du J, Wang Z, Yuan W, Qiao Y, Zhang M, Zhang J, Gao S, Yin J, Sun B, Zhu T (2007) BMP-6 promotes E-cadherin expression through repressing delta EF1 in breast cancer cells. BMC Cancer 7:211. doi:10.1186/1471-2407-7-211
11. Yang S, Du J, Wang Z, Yan J, Yuan W, Zhang J, Zhu T (2009) Dual mechanism of δEF1 expression regulated by bone morphogenetic protein-6 in breast cancer. Int J Biochem Cell Biol 41:853-861. doi:10.1016/j.biocel.2008.08.030
12. Ye L, Bokobza S, Li J, Moazzam M, Chen J, Mansel RE, Jiang WG (2010) Bone morphogenetic protein-10 (BMP-10) inhibits aggressiveness of breast cancer cells and correlates with poor prognosis in breast cancer. Cancer Sci 101:2137-2144. doi:10.1111/j.1349-7006.2010.01648.x
13. Hanavadi S, Martin TA, Watkins G, Mansel RE, Jiang WG (2007) The role of growth differentiation factor-9 (GDF-9) and its analog, GDF-9b/BMP-15, in human breast cancer. Ann Surg Oncol 14:2159-2166. doi:10.1245/s10434-007-9397-5 (Pubitemid 46988265)
14. Cheng H, Jiang W, Phillips FM, Haydon RC, Peng Y, Zhou L, Luu HH, An N, Breyer B, Vanichakarn P, Szatkowski JP, Park JY, He TC (2003) Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs). J Bone Joint Surg Am 85-A:1544-1552 (Pubitemid 36951140)
15. Kang Q, Sun MH, Cheng H, Peng Y, Montag AG, Deyrup AT, Jiang W, Luu HH, Luo J, Szatkowski JP, Vanichakarn P, Park JY, Li Y, Haydon RC, He TC (2004) Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adenovirus-mediated gene delivery. Gene Ther 11:1312-1320. doi:10.1038/sj.gt.3302298 (Pubitemid 39213996)
16. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B (1998) A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95:2509-2514 (Pubitemid 28145972)
17. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, Sharff KA, Luu HH, Haydon RC, Kinzler KW, Vogelstein B, He TC (2007) A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2:1236-1247. doi:10.1038/nprot.2007.135 (Pubitemid 46908240)
18. Luo Q, Kang Q, Song WX, Luu HH, Luo X, An N, Luo J, Deng ZL, Jiang W, Yin H, Chen J, Sharff KA, Tang N, Bennett E, Haydon RC, He TC (2007) Selection and validation of optimal siRNA target sites for RNAi-mediated gene silencing. Gene 395:160-169. doi:10.1016/j.gene.2007.02.030 (Pubitemid 46670640)
19. Su Y, Luo X, He BC, Wang Y, Chen L, Zuo GW, Liu B, Bi Y, Huang J, Zhu GH, He Y, Kang Q, Luo J, Shen J, Chen J, Jin X, Haydon RC, He TC, Luu HH (2009) Establishment and characterization of a new highly metastatic human osteosarcoma cell line. Clin Exp Metastasis 26:599-610. doi:10.1007/s10585-009-9259-6
20. Bi Y, Huang J, He Y, Zhu GH, Su Y, He BC, Luo J, Wang Y, Kang Q, Luo Q, Chen L, Zuo GW, Jiang W, Liu B, Shi Q, Tang M, Zhang BQ, Weng Y, Huang A, Zhou L, Feng T, Luu HH, Haydon RC, He TC, Tang N (2009) Wnt antagonist SFRP3 inhibits the differentiation of mouse hepatic progenitor cells. J Cell Biochem 108:295-303. doi:10.1002/jcb.22254
21. Fidler IJ (2003) The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 3:453-458. doi:10.1038/nrc1098
22. Wang X, Lu H, Urvalek AM, Li T, Yu L, Lamar J, Dipersio CM, Feustel PJ and Zhao J (2010) KLF8 promotes human breast cancer cell invasion and metastasis by transcriptional activation of MMP9. Oncogene. doi:10.1038/onc.2010.563
23. Sapkota D, Bruland O, Costea DE, Haugen H, Vasstrand EN and Ibrahim SO (2010) S100A14 regulates the invasive potential of oral squamous cell carcinoma derived cell-lines in vitro by modulating expression of matrix metalloproteinases, MMP1 and MMP9. Eur J Cancer. doi:10.1016/j.ejca.2010.10.012
24. Dewan MZ, Ahmed S, Iwasaki Y, Ohba K, Toi M, Yamamoto N (2006) Stromal cell-derived factor-1 and CXCR4 receptor interaction in tumor growth and metastasis of breast cancer. Biomed Pharmacother 60:273-276. doi:10.1016/j.biopha.2006.06.004 (Pubitemid 44223937)
25. Shepherd TG, Theriault BL, Nachtigal MW (2008) Autocrine BMP4 signalling regulates ID3 proto-oncogene expression in human ovarian cancer cells. Gene 414:95-105. doi:10.1016/j.gene.2008.02.015
26. Theriault BL, Shepherd TG, Mujoomdar ML, Nachtigal MW (2007) BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis 28:1153-1162. doi:10.1093/carcin/bgm015 (Pubitemid 47062673)
27. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, Brem H, Olivi A, Dimeco F, Vescovi AL (2006) Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444:761-765. doi:10.1038/nature05349 (Pubitemid 44949605)
28. 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. doi:10.1038/sj.onc.1210182 (Pubitemid 46920167)
29. Hjertner O, Hjorth-Hansen H, Borset M, Seidel C, Waage A, Sundan A (2001) Bone morphogenetic protein-4 inhibits proliferation and induces apoptosis of multiple myeloma cells. Blood 97:516-522 (Pubitemid 32060339)
30. Malemud CJ (2006) Matrix metalloproteinases (MMPs) in health and disease: an overview. Front Biosci 11:1696-1701. doi:10.2741/1915
31. Hanemaaijer R, Verheijen JH, Maguire TM, Visser H, Toet K, McDermott E, O'Higgins N, Duffy MJ (2000) Increased gelatinase-A and gelatinase-B activities in malignant vs. benign breast tumors. Int J Cancer 86:204-207. doi:10.1002/(SICI)1097-0215(20000415)86:2〈204:AID-IJC9〉3.0.CO;2-6 (Pubitemid 30180815)
32. London CA, Sekhon HS, Arora V, Stein DA, Iversen PL, Devi GR (2003) A novel antisense inhibitor of MMP-9 attenuates angiogenesis, human prostate cancer cell invasion and tumorigenicity. Cancer Gene Ther 10:823-832. doi:10.1038/sj.cgt.7700642 (Pubitemid 37420041)
33. Riedel F, Gotte K, Schwalb J, Bergler W, Hormann K (2000) Expression of 92-kDa type IV collagenase correlates with angiogenic markers and poor survival in head and neck squamous cell carcinoma. Int J Oncol 17:1099-1105
34. Scorilas A, Karameris A, Arnogiannaki N, Ardavanis A, Bassilopoulos P, Trangas T, Talieri M (2001) Overexpression of matrix-metalloproteinase-9 in human breast cancer: a potential favourable indicator in node-negative patients. Br J Cancer 84:1488-1496. doi:10.1054/bjoc.2001.1810 (Pubitemid 32579341)
35. Wyatt CA, Geoghegan JC, Brinckerhoff CE (2005) Short hairpin RNA-mediated inhibition of matrix metalloproteinase-1 in MDA-231 cells: effects on matrix destruction and tumor growth. Cancer Res 65:11101-11108. doi:10.1158/0008-5472. CAN-05-2446 (Pubitemid 41713381)
36. Daniele A, Zito AF, Giannelli G, Divella R, Asselti M, Mazzocca A, Paradiso A, Quaranta M (2010) Expression of metalloproteinases MMP-2 and MMP-9 in sentinel lymph node and serum of patients with metastatic and non-metastatic breast cancer. Anticancer Res 30:3521-3527
37. Stankovic S, Konjevic G, Gopcevic K, Jovic V, Inic M, Jurisic V (2010) Activity of MMP-2 and MMP-9 in sera of breast cancer patients. Pathol Res Pract 206:241-247. doi:10.1016/j.prp.2009.12.003
38. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3:537-549 (Pubitemid 36808649)
39. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J (2005) Genes that mediate breast cancer metastasis to lung. Nature 436:518-524. doi:10.1038/nature03799 (Pubitemid 41112921)
40. Hassan S, Ferrario C, Saragovi U, Quenneville L, Gaboury L, Baccarelli A, Salvucci O, Basik M (2009) The influence of tumor-host interactions in the stromal cell-derived factor-1/CXCR4 ligand/receptor axis in determining metastatic risk in breast cancer. Am J Pathol 175:66-73. doi:10.2353/ajpath. 2009.080948
41. Liang Z, Wu H, Reddy S, Zhu A, Wang S, Blevins D, Yoon Y, Zhang Y, Shim H (2007) Blockade of invasion and metastasis of breast cancer cells via targeting CXCR4 with an artificial microRNA. Biochem Biophys Res Commun 363:542-546. doi:10.1016/j.bbrc.2007.09.007 (Pubitemid 47513664)
42. Li HY, Ren GS, Tan JX (2009) Effect of small interfering RNA targeting CXCR4 on breast cancer angiogenesis. Nan Fang Yi Ke Da Xue Xue Bao 29:954-958
43. Li HY, Ren GS, Tan JX (2009) The effects of shRNA-CXCR4 on breast cancer cells migration and invasion. Sichuan Da Xue Xue Bao Yi Xue Ban 40:393-397
44. Richert MM, Vaidya KS, Mills CN, Wong D, Korz W, Hurst DR, Welch DR (2009) Inhibition of CXCR4 by CTCE-9908 inhibits breast cancer metastasis to lung and bone. Oncol Rep 21:761-767
45. Huang EH, Singh B, Cristofanilli M, Gelovani J, Wei C, Vincent L, Cook KR, Lucci A (2009) A CXCR4 antagonist CTCE-9908 inhibits primary tumor growth and metastasis of breast cancer. J Surg Res 155:231-236. doi:10.1016/j.jss.2008. 06.044
46. Mizell J, Smith M, Li BD, Ampil F, Chu QD (2009) Overexpression of CXCR4 in primary tumor of patients with HER-2 negative breast cancer was predictive of a poor disease-free survival: a validation study. Ann Surg Oncol 16:2711-2716. doi:10.1245/s10434-009-0551-0
47. Andre F, Xia W, Conforti R, Wei Y, Boulet T, Tomasic G, Spielmann M, Zoubir M, Berrada N, Arriagada R, Hortobagyi GN, Hung MC, Pusztai L, Delaloge S, Michiels S, Cristofanilli M (2009) CXCR4 expression in early breast cancer and risk of distant recurrence. Oncologist 14:1182-1188. doi:10.1634/theoncologist. 2009-0161
48. Hiller DJ, Li BD and Chu QD (2010) CXCR4 as a predictive marker for locally advanced breast cancer post-neoadjuvant therapy J Surg Res (1). doi:10.1016/j.jss.2010.04.045
49. Holm NT, Abreo F, Johnson LW, Li BD, Chu QD (2009) Elevated chemokine receptor CXCR4 expression in primary tumors following neoadjuvant chemotherapy predicts poor outcomes for patients with locally advanced breast cancer (LABC). Breast Cancer Res Treat 113:293-299. doi:10.1007/s10549-008-9921-8
50. Chu QD, Holm NT, Madumere P, Johnson LW, Abreo F and Li BD (2010) Chemokine receptor CXCR4 overexpression predicts recurrence for hormone receptor-positive, node-negative breast cancer patients. Surgery. doi:10.1016/j.surg.2010.05.016
51. Zhao Y, Cai Y, Wang YN (2010) RANKL and OPG regulation on bone remodeling. Shanghai Kou Qiang Yi Xue 19:443-446
52. Boyce BF, Xing L (2008) Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys 473:139-146. doi:10.1016/j.abb.2008.03.018
53. Kearns AE, Khosla S, Kostenuik PJ (2008) Receptor activator of nuclear factor kappaB ligand and osteoprotegerin regulation of bone remodeling in health and disease. Endocr Rev 29:155-192. doi:10.1210/er.2007-0014 (Pubitemid 351519689)
54. Gazzerro E, Gangji V, Canalis E (1998) Bone morphogenetic proteins induce the expression of noggin, which limits their activity in cultured rat osteoblasts. J Clin Invest 102:2106-2114. doi:10.1172/JCI3459 (Pubitemid 29018817)
55. Feeley BT, Krenek L, Liu N, Hsu WK, Gamradt SC, Schwarz EM, Huard J, Lieberman JR (2006) Overexpression of noggin inhibits BMP-mediated growth of osteolytic prostate cancer lesions. Bone 38:154-166. doi:10.1016/j.bone.2005.07. 015 (Pubitemid 43165781)
56. Feeley BT, Liu NQ, Conduah AH, Krenek L, Roth K, Dougall WC, Huard J, Dubinett S, Lieberman JR (2006) Mixed metastatic lung cancer lesions in bone are inhibited by noggin overexpression and Rank:Fc administration. J Bone Miner Res 21:1571-1580. doi:10.1359/jbmr.060706 (Pubitemid 44484602)