Transcriptional network analysis identifies BACH1 as a master regulator of breast cancer bone metastasis

Journal of Biological Chemistry

Volumn 287, Issue 40, 2012, Pages 33533-33544

  Liang, Yajun ^a   Wu, Heng ^b   Lei, Rong ^a   Chong, Robert A ^b   Wei, Yong ^b   Lu, Xin ^b   Tagkopoulos, Ilias ^c   Kung, Sun Yuan ^c   Yang, Qifeng ^d   Hu, Guohong ^a,b   Kang, Yibin ^b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b PRINCETON UNIVERSITY   (United States)

^c Princeton University   (United States)

^d SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BONE METASTASIS; BREAST CANCER; BREAST CANCER CELLS; COMPUTATIONAL APPROACH; ECTOPIC EXPRESSIONS; EXPERIMENTAL VALIDATIONS; FUNCTIONAL GENOMIC ANALYSIS; GENE REGULATORY NETWORKS; LEUCINE-ZIPPER TRANSCRIPTION FACTORS; MASTER REGULATORS; MOLECULAR DETERMINANTS; PATHOLOGICAL PROCESS; TARGET GENES; TRANSCRIPTIONAL NETWORKS;

BONE; DISEASES; GENES; TRANSCRIPTION FACTORS;

PATHOLOGY;

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CHEMOKINE RECEPTOR CXCR4; HYPOXIA INDUCIBLE FACTOR 1; INTERSTITIAL COLLAGENASE; PROTEIN BACH1; SMAD4 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACH1 GENE; BONE METASTASIS; BREAST CANCER; CANCER RECURRENCE; COMPUTER SIMULATION; CONTROLLED STUDY; CXCR4 GENE; FEMALE; FUNCTIONAL GENOMICS; GENE; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; MMP1 GENE; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RECURRENCE RISK; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; VALIDATION PROCESS;

ANIMALS; ANOXIA; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BONE AND BONES; BONE NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MATRIX METALLOPROTEINASE 1; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; PROMOTER REGIONS, GENETIC; SMAD PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84866939028     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.392332     Document Type: Article

References (45)

1. Jemal, A., Bray, F., Center, M. M., Ferlay, J., Ward, E., and Forman, D. (2011) Global cancer statistics. CA-Cancer J. Clin. 61, 69-90
2. van de Vijver, M. J., He, Y. D., van't Veer, L. J., Dai, H., Hart, A. A., Voskuil, D. W., Schreiber, G. J., Peterse, J. L., Roberts, C., Marton, M. J., Parrish, M., Atsma, D., Witteveen, A., Glas, A., Delahaye, L., van der Velde, T., Bartelink, H., Rodenhuis, S., Rutgers, E. T., Friend, S. H., and Bernards, R. (2002) A gene expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999-2009 (Pubitemid 35461656)
3. Ramaswamy, S., Ross, K. N., Lander, E. S., and Golub, T. R. (2003) A molecular signature of metastasis in primary solid tumors. Nat. Genet. 33, 49-54 (Pubitemid 36068681)
4. Kang, Y., Siegel, P. M., Shu, W., Drobnjak, M., Kakonen, S. M., Cordón-Cardo, C., Guise, T. A., and Massagué, J. (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549 (Pubitemid 36808649)
5. van 't Veer, L. J., Dai, H., van de Vijver, M. J., He, Y. D., Hart, A. A., Mao, M., Peterse, H. L., van der Kooy, K., Marton, M. J., Witteveen, A. T., Schreiber, G. J., Kerkhoven, R. M., Roberts, C., Linsley, P. S., Bernards, R., and Friend, S. H. (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415, 530-536 (Pubitemid 34130608)
6. Minn, A. J., Gupta, G. P., Siegel, P. M., Bos, P. D., Shu, W., Giri, D. D., Viale, A., Olshen, A. B., Gerald, W. L., and Massagué, J. (2005) Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524 (Pubitemid 41112921)
7. Bos, P. D., Zhang, X. H., Nadal, C., Shu, W., Gomis, R. R., Nguyen, D. X., Minn, A. J., van de Vijver, M. J., Gerald, W. L., Foekens, J. A., and Massagué, J. (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005-1009
8. Wang, Y., Klijn, J. G., Zhang, Y., Sieuwerts, A. M., Look, M. P., Yang, F., Talantov, D., Timmermans, M., Meijer-van Gelder, M. E., Yu, J., Jatkoe, T., Berns, E. M., Atkins, D., and Foekens, J. A. (2005) Gene expression profiles to predict distant metastasis of lymph node-negative primary breast cancer. Lancet 365, 671-679 (Pubitemid 40260888)
9. Butte, A. J., Tamayo, P., Slonim, D., Golub, T. R., and Kohane, I. S. (2000) Discovering functional relationships between RNA expression and chemotherapeutic susceptibility using relevance networks. Proc. Natl. Acad. Sci. U.S.A. 97, 12182-12186
10. Yeung, M. K., Tegnér, J., and Collins, J. J. (2002) Reverse engineering gene networks using singular value decomposition and robust regression. Proc. Natl. Acad. Sci. U.S.A. 99, 6163-6168 (Pubitemid 34493283)
11. Gardner, T. S., di Bernardo, D., Lorenz, D., and Collins, J. J. (2003) Inferring genetic networks and identifying compound mode of action via expression profiling. Science 301, 102-105 (Pubitemid 36801571)
12. Friedman, N., Linial, M., Nachman, I., and Pe'er, D. (2000) Using Bayesian networks to analyze expression data. J. Comput. Biol. 7, 601-620
13. Hartemink, A. J., Gifford, D. K., Jaakkola, T. S., and Young, R. A. (2001) Pacific Symposium on Biocomputing (PSB), Hawaii, January 4-9, 2000, pp. 6422-6433, The National Library of Medicine/National Institutes of Health and the International Society for Computational Biology, Bethesda, MD
14. Butte, A. J., and Kohane, I. S. (2000) Pacific Symposium on Biocomputing (PSB), Hawaii, January 3-7, 2001, pp. 5418-5429, The National Library of Medicine/National Institutes of Health and the International Society for Computational Biology, Bethesda, MD
15. Huynh-Thu, V. A., Irrthum, A., Wehenkel, L., and Geurts, P. (2010) Inferring regulatory networks from expression data using tree-based methods. PloS One 5, e12776
16. Rhodes, D. R., Kalyana-Sundaram, S., Mahavisno, V., Barrette, T. R., Ghosh, D., and Chinnaiyan, A. M. (2005) Mining for regulatory programs in the cancer transcriptome. Nat. Genet. 37, 579-583 (Pubitemid 40770410)
17. Elkon, R., Linhart, C., Sharan, R., Shamir, R., and Shiloh, Y. (2003) Genome-wide in silico identification of transcriptional regulators controlling the cell cycle in human cells. Genome Res. 13, 773-780 (Pubitemid 36621737)
18. Margolin, A. A., Nemenman, I., Basso, K., Wiggins, C., Stolovitzky, G., Dalla Favera, R., and Califano, A. (2006) BMC Bioinformatics 7, S7
19. Margolin, A. A., Wang, K., Lim, W. K., Kustagi, M., Nemenman, I., and Califano, A. (2006) Reverse engineering cellular networks. Nature Protoc. 1, 662-671
20. Lefebvre, C., Rajbhandari, P., Alvarez, M. J., Bandaru, P., Lim, W. K., Sato, M., Wang, K., Sumazin, P., Kustagi, M., Bisikirska, B. C., Basso, K., Beltrao, P., Krogan, N., Gautier, J., Dalla-Favera, R., and Califano, A. (2010) A human B-cell interactome identifies MYB and FOXM1 as master regulators of proliferation in germinal centers. Mol. Syst. Biol. 6, 377
21. Basso, K., Margolin, A. A., Stolovitzky, G., Klein, U., Dalla-Favera, R., and Califano, A. (2005) Reverse engineering of regulatory networks in human B cells. Nat. Genet. 37, 382-390
22. Taylor, R. C., Acquaah-Mensah, G., Singhal, M., Malhotra, D., and Biswal, S. (2008) Network inference algorithms elucidate Nrf2 regulation of mouse lung oxidative stress. PLoS Comput. Biol. 4, e1000166
23. Carro, M. S., Lim, W. K., Alvarez, M. J., Bollo, R. J., Zhao, X., Snyder, E. Y., Sulman, E. P., Anne, S. L., Doetsch, F., Colman, H., Lasorella, A., Aldape, K., Califano, A., and Iavarone, A. (2010) The transcriptional network for mesenchymal transformation of brain tumors. Nature 463, 318-325
24. Lim, W. K., Lyashenko, E., and Califano, A. (2009) Pacific Symposium on Biocomputing (PSB), Hawaii, January 5-9, 2009, pp. 14504-14515, The National Library of Medicine/National Institutes of Health and the International Society for Computational Biology, Bethesda, MD
25. Lu, X., Yan, C. H., Yuan, M., Wei, Y., Hu, G., and Kang, Y. (2010) In vivo dynamics and distinct functions of hypoxia in primary tumor growth and organotropic metastasis of breast cancer. Cancer Res. 70, 3905-3914
26. Korpal, M., Yan, J., Lu, X., Xu, S., Lerit, D. A., and Kang, Y. (2009) Imaging transforming growth factor-β signaling dynamics and therapeutic response in breast cancer bone metastasis. Nature Med. 15, 960-966
27. Mohammad, K. S., Javelaud, D., Fournier, P. G., Niewolna, M., McKenna, C. R., Peng, X. H., Duong, V., Dunn, L. K., Mauviel, A., and Guise, T. A. (2011) TGF-β-RI kinase inhibitor SD-208 reduces the development and progression of melanoma bone metastases. Cancer Res. 71, 175-184
28. Dunn, L. K., Mohammad, K. S., Fournier, P. G., McKenna, C. R., Davis, H. W., Niewolna, M., Peng, X. H., Chirgwin, J. M., and Guise, T. A. (2009) Hypoxia and TGF-β drive breast cancer bone metastases through parallel signaling pathways in tumor cells and the bone microenvironment. PloS One 4, e6896
29. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., and Mesirov, J. P. (2005) Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550 (Pubitemid 41528093)
30. Tagkopoulos, I., Slavov, N., and Kung, S. Y. (2005) Fifth IEEE Symposium on Bioinformatics and Bioengineering (BIBE'05), Washington, DC, October 19-21, 2005
31. Matys, V., Fricke, E., Geffers, R., Gössling, E., Haubrock, M., Hehl, R., Hornischer, K., Karas, D., Kel, A. E., Kel-Margoulis, O. V., Kloos, D. U., Land, S., Lewicki-Potapov, B., Michael, H., Münch, R., Reuter, I., Rotert, S., Saxel, H., Scheer, M., Thiele, S., and Wingender, E. (2003) TRANSFAC: Transcriptional regulation, from patterns to profiles. Nucleic Acids Res. 31, 374-378 (Pubitemid 36150406)
32. Nelson, J. D., Denisenko, O., and Bomsztyk, K. (2006) Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nature Protoc. 1, 179-185
33. Kang, Y., He, W., Tulley, S., Gupta, G. P., Serganova, I., Chen, C. R., Manova-Todorova, K., Blasberg, R., Gerald, W. L., and Massagué, J. (2005) Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc. Natl. Acad. Sci. U.S.A. 102, 13909-13914 (Pubitemid 41377677)
34. Cheng, Y., and Church, G. M. (2000) Biclustering of expression data. Proc. Int. Conf. Intell. Syst. Mol. Biol. 8, 93-103
35. Harris, A. L. (2002) Hypoxia-a key regulatory factor in tumor growth. Nat. Rev. Cancer 2, 38-47
36. Zhong, H., De Marzo, A. M., Laughner, E., Lim, M., Hilton, D. A., Zagzag, D., Buechler, P., Isaacs, W. B., Semenza, G. L., and Simons, J. W. (1999) Overexpression of hypoxia-inducible factor 1α in common human cancers and their metastases. Cancer Res. 59, 5830-5835
37. Hintze, K. J., Katoh, Y., Igarashi, K., and Theil, E. C. (2007) Bach1 repression of ferritin and thioredoxin reductase1 is heme-sensitive in cells and in vitro and coordinates expression with heme oxygenase1, β-globin, and NADP(H) quinone(oxido) reductase1. J. Biol. Chem. 282, 34365-34371 (Pubitemid 350159431)
38. Oyake, T., Itoh, K., Motohashi, H., Hayashi, N., Hoshino, H., Nishizawa, M., Yamamoto, M., and Igarashi, K. (1996) Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell. Biol. 16, 6083-6095 (Pubitemid 26360968)
39. Sun, J., Brand, M., Zenke, Y., Tashiro, S., Groudine, M., and Igarashi, K. (2004) Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc. Natl. Acad. Sci. U.S.A. 101, 1461-1466 (Pubitemid 38234177)
40. Warnatz, H. J., Schmidt, D., Manke, T., Piccini, I., Sultan, M., Borodina, T., Balzereit, D., Wruck, W., Soldatov, A., Vingron, M., Lehrach, H., and Yaspo, M. L. (2011) The BTB and CNC homology 1 (BACH1) target genes are involved in the oxidative stress response and in control of the cell cycle. J. Biol. Chem. 286, 23521-23532
41. Toki, T., Katsuoka, F., Kanezaki, R., Xu, G., Kurotaki, H., Sun, J., Kamio, T., Watanabe, S., Tandai, S., Terui, K., Yagihashi, S., Komatsu, N., Igarashi, K., Yamamoto, M., and Ito, E. (2005) Transgenic expression of BACH1 transcription factor results in megakaryocytic impairment. Blood 105, 3100-3108
42. Alvarez, A., and Woolf, P. J. (2011) RegNetB: Predicting relevant regulator-gene relationships in localized prostate tumor samples. BMC Bioinformatics 12, 243
43. Yun, J., Frankenberger, C. A., Kuo, W. L., Boelens, M. C., Eves, E. M., Cheng, N., Liang, H., Li, W. H., Ishwaran, H., Minn, A. J., and Rosner, M. R. (2011) Signaling pathway for RKIP and Let-7 regulates and predicts metastatic breast cancer. EMBO J. 30, 4500-4514
44. Egeblad, M., and Werb, Z. (2002) New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174 (Pubitemid 37328786)
45. Lu, X., Wang, Q., Hu, G., Van Poznak, C., Fleisher, M., Reiss, M., Massagué, J., and Kang, Y. (2009) ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis. Genes Dev. 23, 1882-1894