Analysis of BMP4 and BMP7 signaling in breast cancer cells unveils time-dependent transcription patterns and highlights a common synexpression group of genes

BMC Medical Genomics

Volumn 4, Issue , 2011, Pages

  Rodriguez Martinez, Alejandra ^a   Alarmo, Emma Leena ^a   Saarinen, Lilli ^b   Ketolainen, Johanna ^a   Nousiainen, Kari ^b   Hautaniemi, Sampsa ^b   Kallioniemi, Anne ^a  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

BMP4; BMP7; bone morphogenetic protein; breast cancer; expression microarray

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; OSTEOGENIC PROTEIN 1; BMP4 PROTEIN, HUMAN; BMP7 PROTEIN, HUMAN; LIGAND;

ARTICLE; BREAST CANCER; CANCER CELL; CELL FUNCTION; CELL METABOLISM; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE SEQUENCE; GENE TARGETING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MICROARRAY; TIME SERIES ANALYSIS; TRANSCRIPTION REGULATION; TREATMENT RESPONSE; BREAST TUMOR; DRUG EFFECT; FEMALE; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TIME; TUMOR CELL LINE;

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 7; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMICS; HUMANS; LIGANDS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 82055175800     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/1755-8794-4-80     Document Type: Article

References (51)

1. TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Schmierer B, Hill CS, Nat Rev Mol Cell Biol 2007 8 970 982 10.1038/nrm2297 18000526 (Pubitemid 350174642)
2. Signal transduction of bone morphogenetic protein receptors. Nohe A, Keating E, Knaus P, Petersen NO, Cell Signal 2004 16 291 299 10.1016/j.cellsig.2003.08.011 14687659 (Pubitemid 37542404)
3. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Derynck R, Zhang YE, Nature 2003 425 577 584 10.1038/nature02006 14534577 (Pubitemid 37280136)
4. TGFbeta and Wnt pathway cross-talk. Attisano L, Labbe E, Cancer Metastasis Rev 2004 23 53 61 15000149
5. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Miyazono K, Maeda S, Imamura T, Cytokine Growth Factor Rev 2005 16 251 263 10.1016/j.cytogfr.2005.01.009 15871923 (Pubitemid 40910315)
6. Cross-talk between the bone morphogenetic protein pathway and other major signaling pathways results in tightly regulated cell-specific outcomes. Herpin A, Cunningham C, Febs J 2007 274 2977 2985 10.1111/j.1742-4658.2007.05840.x 17521337 (Pubitemid 46849089)
7. Novel regulators of bone formation: molecular clones and activities. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA, Science 1988 242 1528 1534 10.1126/science.3201241 3201241 (Pubitemid 19023695)
8. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Hogan BL, Genes Dev 1996 10 1580 1594 10.1101/gad.10.13.1580 8682290 (Pubitemid 26268864)
9. Bone morphogenetic proteins and cancer: review of the literature. Thawani JP, Wang AC, Than KD, Lin CY, La Marca F, Park P, Neurosurgery 2010 66 233 246 discussion 246 10.1227/01.NEU.0000363722.42097.C2 20042986
10. The Yin and Yang of bone morphogenetic proteins in cancer. Singh A, Morris RJ, Cytokine Growth Factor Rev 2010 21 299 313 10.1016/j.cytogfr.2010.06. 003 20688557
11. Bone morphogenetic proteins in breast cancer: dual role in tumourigenesis? Alarmo EL, Kallioniemi A, Endocr Relat Cancer 2010 17 123 139 10.1677/ERC-09-0273 20335308
12. A comprehensive expression survey of bone morphogenetic proteins in breast cancer highlights the importance of BMP4 and BMP7. Alarmo EL, Kuukasjarvi T, Karhu R, Kallioniemi A, Breast Cancer Res Treat 2007 103 239 246 10.1007/s10549-006-9362-1 17004110 (Pubitemid 46789146)
13. Differential expression and regulation of bone morphogenetic protein 7 in breast cancer. Schwalbe M, Sanger J, Eggers R, Naumann A, Schmidt A, Hoffken K, Clement JH, Int J Oncol 2003 23 89 95 12792780
14. Parallel inhibition of cell growth and induction of cell migration and invasion in breast cancer cells by bone morphogenetic protein 4. Ketolainen JM, Alarmo EL, Tuominen VJ, Kallioniemi A, Breast Cancer Res Treat 2010
15. Bone morphogenetic protein 7 expression associates with bone metastasis in breast carcinomas. Alarmo EL, Korhonen T, Kuukasjarvi T, Huhtala H, Holli K, Kallioniemi A, Ann Oncol 2008 19 308 314 10.1093/annonc/mdm453 17895257 (Pubitemid 351201712)
16. Bone morphogenetic protein 7 is widely overexpressed in primary breast cancer. Alarmo EL, Rauta J, Kauraniemi P, Karhu R, Kuukasjarvi T, Kallioniemi A, Genes Chromosomes Cancer 2006 45 411 419 10.1002/gcc.20307 16419056 (Pubitemid 43346773)
17. Lack of noggin expression by cancer cells is a determinant of the osteoblast response in bone metastases. Schwaninger R, Rentsch CA, Wetterwald A, van der Horst G, van Bezooijen RL, van der Pluijm G, Lowik CW, Ackermann K, Pyerin W, Hamdy FC, et al. Am J Pathol 2007 170 160 175 10.2353/ajpath.2007. 051276 17200191 (Pubitemid 47339197)
18. Bone morphogenetic protein 7 in the development and treatment of bone metastases from breast cancer. Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, Que I, Schwaninger R, Rentsch C, Ten Dijke P, Cleton-Jansen AM, Driouch K, et al. Cancer Res 2007 67 8742 8751 10.1158/0008-5472.CAN-06-2490 17875715 (Pubitemid 47437450)
19. Bone morphogenetic protein-4 abrogates lumen formation by mammary epithelial cells and promotes invasive growth. Montesano R, Biochem Biophys Res Commun 2007 353 817 822 10.1016/j.bbrc.2006.12.109 17189614 (Pubitemid 46048745)
20. Bone morphogenetic protein-4 induced by NDRG2 expression inhibits MMP-9 activity in breast cancer cells. Shon SK, Kim A, Kim JY, Kim KI, Yang Y, Lim JS, Biochem Biophys Res Commun 2009 385 198 203 10.1016/j.bbrc.2009.05.038 19450561
21. BMP7 influences proliferation, migration, and invasion of breast cancer cells. Alarmo EL, Parssinen J, Ketolainen JM, Savinainen K, Karhu R, Kallioniemi A, Cancer Lett 2009 275 35 43 10.1016/j.canlet.2008.09.028 18980801
22. csbl.go: Semantic similarity based on Gene Ontology. http://csbi.ltdk. helsinki.fi/csbl.go
23. Model based clustering, discriminant analysis, and density estimation. Fraley C, Raftery AE, J Am Stat Assoc 2002 97 611 631 10.1198/016214502760047131
24. Model-based clustering and data transformations for gene expression data. Yeung KY, Fraley C, Murua A, Raftery AE, Ruzzo WL, Bioinformatics 2001 17 977 987 10.1093/bioinformatics/17.10.977 11673243 (Pubitemid 32998635)
25. Large-scale data integration framework provides a comprehensive view on glioblastoma multiforme. Ovaska K, Laakso M, Haapa-Paananen S, Louhimo R, Chen P, Aittomaki V, Valo E, Nunez-Fontarnau J, Rantanen V, Karinen S, et al. Genome Med 2010 2 65 10.1186/gm186 20822536
26. R: A language and environment for statistical computing. R-Development-Core-Team, Vienna, Austria: R Foundation for Statistical Computing 2011
27. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A, J Biol Chem 1999 274 19838 19845 10.1074/jbc.274.28.19838 10391928 (Pubitemid 29327766)
28. Id2 and Id3 define the potency of cell proliferation and differentiation responses to transforming growth factor beta and bone morphogenetic protein. Kowanetz M, Valcourt U, Bergstrom R, Heldin CH, Moustakas A, Mol Cell Biol 2004 24 4241 4254 10.1128/MCB.24.10.4241-4254.2004 15121845 (Pubitemid 41070996)
29. Bone morphogenetic protein 2 (BMP-2) induces sequential changes of Id gene expression in the breast cancer cell line MCF-7. Clement JH, Marr N, Meissner A, Schwalbe M, Sebald W, Kliche KO, Hoffken K, Wolfl S, J Cancer Res Clin Oncol 2000 126 271 279 10.1007/s004320050342 10815762 (Pubitemid 30246248)
30. Differential expression of cancer-related genes by single and permanent exposure to bone morphogenetic protein 2. Steinert S, Kroll TC, Taubert I, Pusch L, Hortschansky P, Hoffken K, Wolfl S, Clement JH, J Cancer Res Clin Oncol 2008 134 1237 1245 10.1007/s00432-008-0396-0 18446370
31. Bone morphogenetic protein 6 (BMP6) and BMP7 inhibit estrogen-induced proliferation of breast cancer cells by suppressing p38 mitogen-activated protein kinase activation. Takahashi M, Otsuka F, Miyoshi T, Otani H, Goto J, Yamashita M, Ogura T, Makino H, Doihara H, J Endocrinol 2008 199 445 455 10.1677/JOE-08-0226 18780779
32. Controlling of bone morphogenetic protein signaling. Zeng S, Chen J, Shen H, Cell Signal 2010 22 888 893 10.1016/j.cellsig.2009.12.007 20060893
33. Smad transcription factors. Massague J, Seoane J, Wotton D, Genes Dev 2005 19 2783 2810 10.1101/gad.1350705 16322555 (Pubitemid 41739965)
34. Regulation of Notch signaling genes during BMP2-induced differentiation of osteoblast precursor cells. de Jong DS, Steegenga WT, Hendriks JM, van Zoelen EJ, Olijve W, Dechering KJ, Biochem Biophys Res Commun 2004 320 100 107 10.1016/j.bbrc.2004.05.150 15207708 (Pubitemid 38781789)
35. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A, Mol Biol Cell 2005 16 1987 2002 10.1091/mbc.E04-08-0658 15689496 (Pubitemid 40471965)
36. Bone morphogenetic proteins. Chen D, Zhao M, Mundy GR, Growth Factors 2004 22 233 241 10.1080/08977190412331279890 15621726 (Pubitemid 40136452)
37. Bone morphogenetic proteins and their antagonists. Gazzerro E, Canalis E, Rev Endocr Metab Disord 2006 7 51 65 17029022 (Pubitemid 46044349)
38. Global gene expression profiling and cluster analysis in Xenopus laevis. Baldessari D, Shin Y, Krebs O, Konig R, Koide T, Vinayagam A, Fenger U, Mochii M, Terasaka C, Kitayama A, et al. Mech Dev 2005 122 441 475 10.1016/j.mod.2004. 11.007 15763214 (Pubitemid 40341920)
39. Transcriptional regulation of BMP4 synexpression in transgenic Xenopus. Karaulanov E, Knochel W, Niehrs C, Embo J 2004 23 844 856 10.1038/sj.emboj. 7600101 14963489 (Pubitemid 38418751)
40. Id helix-loop-helix proteins in cell growth and differentiation. Norton JD, Deed RW, Craggs G, Sablitzky F, Trends Cell Biol 1998 8 58 65 9695810 (Pubitemid 28056812)
41. A role for Id proteins in mammary gland physiology and tumorigenesis. de Candia P, Benera R, Solit DB, Adv Cancer Res 2004 92 81 94 15530557 (Pubitemid 39458113)
42. The BMP antagonists chordin and noggin have essential but redundant roles in mouse mandibular outgrowth. Stottmann RW, Anderson RM, Klingensmith J, Dev Biol 2001 240 457 473 10.1006/dbio.2001.0479 11784076 (Pubitemid 34056504)
43. Bone morphogenetic protein (BMP)-6 signaling and BMP antagonist noggin in prostate cancer. Haudenschild DR, Palmer SM, Moseley TA, You Z, Reddi AH, Cancer Res 2004 64 8276 8284 10.1158/0008-5472.CAN-04-2251 15548695 (Pubitemid 39491765)
44. The role and target potential of protein tyrosine phosphatases in cancer. Yi T, Lindner D, Curr Oncol Rep 2008 10 114 121 10.1007/s11912-008-0019-6 18377824 (Pubitemid 351395471)
45. Inside the human cancer tyrosine phosphatome. Julien SG, Dube N, Hardy S, Tremblay ML, Nat Rev Cancer 2011 11 35 49 10.1038/nrc2980 21179176
46. Receptor protein-tyrosine phosphatase gamma is a candidate tumor suppressor gene at human chromosome region 3p21. LaForgia S, Morse B, Levy J, Barnea G, Cannizzaro LA, Li F, Nowell PC, Boghosian-Sell L, Glick J, Weston A, et al. Proc Natl Acad Sci USA 1991 88 5036 5040 10.1073/pnas.88.11.5036 1711217 (Pubitemid 21914678)
47. Function and regulatory mechanisms of the candidate tumor suppressor receptor protein tyrosine phosphatase gamma (PTPRG) in breast cancer cells. Shu ST, Sugimoto Y, Liu S, Chang HL, Ye W, Wang LS, Huang YW, Yan P, Lin YC, Anticancer Res 2010 30 1937 1946 20651337
48. Function analysis of estrogenically regulated protein tyrosine phosphatase gamma (PTPgamma) in human breast cancer cell line MCF-7. Liu S, Sugimoto Y, Sorio C, Tecchio C, Lin YC, Oncogene 2004 23 1256 1262 10.1038/sj.onc.1207235 14676845 (Pubitemid 38297180)
49. Mammalian MAP kinase signalling cascades. Chang L, Karin M, Nature 2001 410 37 40 10.1038/35065000 11242034 (Pubitemid 32225829)
50. The PAC-1 dual specificity phosphatase predicts poor outcome in serous ovarian carcinoma. Givant-Horwitz V, Davidson B, Goderstad JM, Nesland JM, Trope CG, Reich R, Gynecol Oncol 2004 93 517 523 10.1016/j.ygyno.2004.03.009 15099972 (Pubitemid 38507628)
51. Suppression of dual-specificity phosphatase-2 by hypoxia increases chemoresistance and malignancy in human cancer cells. Lin SC, Chien CW, Lee JC, Yeh YC, Hsu KF, Lai YY, Lin SC, Tsai SJ, J Clin Invest 2011 121 1905 1916 10.1172/JCI44362 21490398