Multimodality imaging of TGFβ signaling in breast cancer metastases

FASEB Journal

Volumn 23, Issue 8, 2009, Pages 2662-2672

  Serganova, Inna ^a   Moroz, Ekaterina ^a   Vider, Jelena ^a   Gogiberidze, George ^a   Moroz, Maxim ^a   Pillarsetty, Nagavarakishore ^a   Doubrovin, Michael ^a   Minn, Andy ^a,b   Thaler, Howard T ^a   Massague, Joan ^a   Gelovani, Juri ^a,c   Blasberg, Ronald ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Bioluminescence; Bone resorption; FEAU; Green fluorescent protein; Herpes simplex virus type one thymidine kinase; Positron emission tomography; Smads complex

Indexed keywords

5 ETHYL 2' FLUOROURACIL ARABINOSIDE; 5 ETHYL 2' FLUOROURACIL ARABINOSIDE F 18; COELENTERAZINE; DIAGNOSTIC AGENT; FIALURIDINE C 14; FIREFLY LUCIFERASE; GREEN FLUORESCENT PROTEIN; RADIOISOTOPE; THYMIDINE H 3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; COMPLEMENTARY DNA; RECOMBINANT PROTEIN;

ADRENAL METASTASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BONE METASTASIS; BREAST ADENOCARCINOMA; CANCER CELL CULTURE; CANCER GROWTH; COST EFFECTIVENESS ANALYSIS; DIAGNOSTIC ACCURACY; HSV1 TK GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTROSPECTION; MONITORING; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; REPRODUCIBILITY; SIGNAL TRANSDUCTION; SPINE METASTASIS; ANIMAL; BONE TUMOR; BREAST TUMOR; CANCER TRANSPLANTATION; COMPUTER ASSISTED TOMOGRAPHY; FEMALE; GENETICS; METABOLISM; METASTASIS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; NUDE MOUSE; TUMOR CELL LINE; XENOGRAFT;

ANIMALIA; SIMPLEXVIRUS;

ANIMALS; BASE SEQUENCE; BONE NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA, COMPLEMENTARY; FEMALE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; LUCIFERASES, FIREFLY; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; NEOPLASM TRANSPLANTATION; POSITRON-EMISSION TOMOGRAPHY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TOMOGRAPHY, X-RAY COMPUTED; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HETEROLOGOUS;

EID: 68849126304     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-126920     Document Type: Article

References (40)

1. Eilon, G., and Mundy, G. R. (1978) Direct resorption of bone by human breast cancer cells in vitro. Nature 276, 726-728 (Pubitemid 9073534)
2. Derynck, R., Akhurst, R. J., and Balmain, A. (2001) TGF-beta signaling in tumor suppression and cancer progression. Nat. Genet. 29, 117-129 (Pubitemid 32952643)
3. Massague, J. (2008) TGFbeta in cancer. Cell 134, 215-230
4. Schmidt-Weber, C. B., and Blaser, K. (2004) Regulation and role of transforming growth factor-beta in immune tolerance induction and inflammation. Curr. Opin. Immunol. 16, 709-716
5. Yin, J. J., Selander, K., Chirgwin, J. M., Dallas, M., Grubbs, B. G., Wieser, R., Massague, J., Mundy, G. R., and Guise, T. A. (1999) TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J. Clin. Invest. 103, 197-206 (Pubitemid 29053137)
6. Chirgwin, J. M., and Guise, T. A. (2000) Molecular mechanisms of tumor-bone interactions in osteolytic metastases. Crit. Rev. Eukaryot. Gene Expr. 10, 159-178
7. Kang, Y., He, W., Tulley, S., Gupta, G. P., Serganova, I., Chen, C. R., Manova-Todorova, K., Blasberg, R., Gerald, W. L., and Massague, 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)
8. Minn, A. J., Kang, Y., Serganova, I., Gupta, G. P., Giri, D. D., Doubrovin, M., Ponomarev, V., Gerald, W. L., Blasberg, R., and Massague, J. (2005) Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J. Clin. Invest. 115, 44-55 (Pubitemid 40385504)
9. Cowey, S., Szafran, A. A., Kappes, J., Zinn, K. R., Siegal, G. P., Desmond, R. A., Kim, H., Evans, L., and Hardy, R. W. (2007) Breast cancer metastasis to bone: evaluation of bioluminescent imaging and microSPECT/CT for detecting bone metastasis in immunodeficient mice. Clin. Exp. Metastasis 24, 389-401 (Pubitemid 47124938)
10. Arvanitis, C., Bendapudi, P. K., Tseng, J. R., Gambhir, S. S., and Felsher, D. W. (2008) (18)F and (18)FDG PET imaging of osteosarcoma to non-invasively monitor in situ changes in cellular proliferation and bone differentiation upon MYC inactivation. Cancer Biol. Ther. 7, 1947-1951
11. Berger, F., Lee, Y. P., Loening, A. M., Chatziioannou, A., Freedland, S. J., Leahy, R., Lieberman, J. R., Belldegrun, A. S., Sawyers, C. L., and Gambhir, S. S. (2002) Whole-body skeletal imaging in mice utilizing microPET: optimization of reproducibility and applications in animal models of bone disease. Eur. J. Nucl. Med. Mol. Imaging 29, 1225-1236 (Pubitemid 34985371)
12. Kang, Y., Siegel, P. M., Shu, W., Drobnjak, M., Kakonen, S. M., Cordon-Cardo, C., Guise, T. A., and Massague, J. (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell. 3, 537-549 (Pubitemid 36808649)
13. Santos, E., Yeh, R., Lee, J., Nikhamin, Y., Punzalan, B., La Perle, K., Larson, S. M., Sadelain, M., and Brentjens, R. J. (2009) Sensitive in vivo imaging of T cells utilizing a membrane bound Gaussia priceps luciferase enzyme. Nat. Med. 15, 338-344
14. Jakubowiak, A., Pouponnot, C., Berguido, F., Frank, R., Mao, S., Massague, J., and Nimer, S. D. (2000) Inhibition of the transforming growth factor beta 1 signaling pathway by the AML1/ ETO leukemia-associated fusion protein. J. Biol. Chem. 275, 40282-40287 (Pubitemid 32064660)
15. Zawel, L., Dai, J. L., Buckhaults, P., Zhou, S., Kinzler, K. W., Vogelstein, B., and Kern, S. E. (1998) Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell 1, 611-617 (Pubitemid 128374697)
16. Wang, S., Wang, Q., Crute, B. E., Melnikova, I. N., Keller, S. R., and Speck, N. A. (1993) Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. Mol. Cell. Biol. 13, 3324-3339 (Pubitemid 23157270)
17. Ponomarev, V., Doubrovin, M., Lyddane, C., Beresten, T., Balatoni, J., Bornman, W., Finn, R., Akhurst, T., Larson, S., Blasberg, R., Sadelain, M., and Tjuvajev, J. G. (2001) Imaging TCR-dependent NFAT-mediated T-cell activation with positron emission tomography in vivo. Neoplasia 3, 480-488 (Pubitemid 33151014)
18. Doubrovin, M., Ponomarev, V., Beresten, T., Balatoni, J., Bornmann, W., Finn, R., Humm, J., Larson, S., Sadelain, M., Blasberg, R., and Gelovani Tjuvajev, J. (2001) Imaging transcriptional regulation of p53-dependent genes with positron emission tomography in vivo. Proc. Natl. Acad. Sci. U. S. A. 98, 9300-9305 (Pubitemid 32743911)
19. Serganova, I., Doubrovin, M., Vider, J., Ponomarev, V., Soghomonyan, S., Beresten, T., Ageyeva, L., Serganov, A., Cai, S., Balatoni, J., Blasberg, R., and Gelovani, J. (2004) Molecular imaging of temporal dynamics and spatial heterogeneity of hypoxia-inducible factor-1 signal transduction activity in tumors in living mice. Cancer Res. 64, 6101-6108 (Pubitemid 39129410)
20. Tjuvajev, J. G., Stockhammer, G., Desai, R., Uehara, H., Watanabe, K., Gansbacher, B., and Blasberg, R. G. (1995) Imaging the expression of transfected genes in vivo. Cancer Res. 55, 6126-6132
21. Tjuvajev, J. G., Finn, R., Watanabe, K., Joshi, R., Oku, T., Kennedy, J., Beattie, B., Koutcher, J., Larson, S., and Blasberg, R. G. (1996) Noninvasive imaging of herpes virus thymidine kinase gene transfer and expression: a potential method for monitoring clinical gene therapy. Cancer Res. 56, 4087-4095 (Pubitemid 26304995)
22. Campbell, R. E., Tour, O., Palmer, A. E., Steinbach, P. A., Baird, G. S., Zacharias, D. A., and Tsien, R. Y. (2002) A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. U. S. A. 99, 7877-7882
23. Zentella, A., Weis, F. M., Ralph, D. A., Laiho, M., and Massague, J. (1991) Early gene responses to transforming growth factor-beta in cells lacking growth-suppressive RB function. Mol. Cell. Biol. 11, 4952-4958 (Pubitemid 21895256)
24. Kingsley, L. A., Fournier, P. G., Chirgwin, J. M., and Guise, T. A. (2007) Molecular biology of bone metastasis. Mol. Cancer Ther. 6, 2609-2617
25. Guise, T. A., Mohammad, K. S., Clines, G., Stebbins, E. G., Wong, D. H., Higgins, L. S., Vessella, R., Corey, E., Padalecki, S., Suva, L., and Chirgwin, J. M. (2006) Basic mechanisms responsible for osteolytic and osteoblastic bone metastases. Clin. Cancer Res. 12, 6213s-6216s (Pubitemid 44703792)
26. Arguello, F., Baggs, R. B., Duerst, R. E., Johnstone, L., McQueen, K., and Frantz, C. N. (1990) Pathogenesis of vertebral metastasis and epidural spinal cord compression. Cancer 65, 98-106 (Pubitemid 20026818)
27. Yoneda, T., Williams, P. J., Hiraga, T., Niewolna, M., and Nishimura, R. (2001) A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast cancer cells and a brain-seeking clone in vivo and in vitro. J. Bone Miner. Res. 16, 1486-1495 (Pubitemid 32675200)
28. Phadke, P. A., Mercer, R. R., Harms, J. F., Jia, Y., Frost, A. R., Jewell, J. L., Bussard, K. M., Nelson, S., Moore, C., Kappes, J. C., Gay, C. V., Mastro, A. M., and Welch, D. R. (2006) Kinetics of metastatic breast cancer cell trafficking in bone. Clin. Cancer Res. 12, 1431-1440
29. Ponomarev, V., Doubrovin, M., Serganova, I., Vider, J., Shavrin, A., Beresten, T., Ivanova, A., Ageyeva, L., Tourkova, V., Balatoni, J., Bornmann, W., Blasberg, R., and Gelovani Tjuvajev, J. (2004) A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging. Eur. J. Nucl. Med. Mol. Imaging 31, 740-751 (Pubitemid 38647915)
30. Fritz, V., Louis-Plence, P., Apparailly, F., Noel, D., Voide, R., Pillon, A., Nicolas, J. C., Muller, R., and Jorgensen, C. (2007) Micro-CT combined with bioluminescence imaging: a dynamic approach to detect early tumor-bone interaction in a tumor osteolysis murine model. Bone 40, 1032-1040 (Pubitemid 46386549)
31. Edinger, M., Cao, Y. A., Hornig, Y. S., Jenkins, D. E., Verneris, M. R., Bachmann, M. H., Negrin, R. S., and Contag, C. H. (2002) Advancing animal models of neoplasia through in vivo bioluminescence imaging. Eur. J. Cancer 38, 2128-2136 (Pubitemid 35223250)
32. Rosol, T. J., Tannehill-Gregg, S. H., LeRoy, B. E., Mandl, S., and Contag, C. H. (2003) Animal models of bone metastasis. Cancer 97, 748-757
33. Yang, M., Baranov, E., Jiang, P., Sun, F. X., Li, X. M., Li, L., Hasegawa, S., Bouvet, M., Al-Tuwaijri, M., Chishima, T., Shimada, H., Moossa, A. R., Penman, S., and Hoffman, R. M. (2000) Whole-body optical imaging of green fluorescent protein- expressing tumors and metastases. Proc. Natl. Acad. Sci. U. S. A. 97, 1206-1211 (Pubitemid 30080837)
34. Kaijzel, E. L., van der Pluijm, G., and Lowik, C. W. (2007) Whole-body optical imaging in animal models to assess cancer development and progression. Clin. Cancer Res. 13, 3490-3497
35. Katsuno, Y., Hanyu, A., Kanda, H., Ishikawa, Y., Akiyama, F., Iwase, T., Ogata, E., Ehata, S., Miyazono, K., and Imamura, T. (2008) Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene 27, 6322-6333
36. Deroose, C. M., De, A., Loening, A. M., Chow, P. L., Ray, P., Chatziioannou, A. F., and Gambhir, S. S. (2007) Multimodality imaging of tumor xenografts and metastases in mice with combined small-animal PET, small-animal CT, and bioluminescence imaging. J. Nucl. Med. 48, 295-303 (Pubitemid 47555357)
37. Winkelmann, C. T., Figueroa, S. D., Rold, T. L., Volkert, W. A., and Hoffman, T. J. (2006) Microimaging characterization of a B16-F10 melanoma metastasis mouse model. Mol. Imaging 5, 105-114 (Pubitemid 44106145)
38. Sugano, Y., Matsuzaki, K., Tahashi, Y., Furukawa, F., Mori, S., Yamagata, H., Yoshida, K., Matsushita, M., Nishizawa, M., Fujisawa, J., and Inoue, K. (2003) Distortion of autocrine transforming growth factor beta signal accelerates malignant potential by enhancing cell growth as well as PAI-1 and VEGF production in human hepatocellular carcinoma cells. Oncogene 22, 2309-2321 (Pubitemid 36566786)
39. Healy, A. M., and Gelehrter, T. D. (1994) Induction of plasminogen activator inhibitor-1 in HepG2 human hepatoma cells by mediators of the acute phase response. J. Biol. Chem. 269, 19095-19100
40. 18F]FFEAU, and other imaging probes. J. Nucl. Med. 49, 637-648