Table of Contents Author Guidelines Submit a Manuscript
Contrast Media & Molecular Imaging
Volume 2017, Article ID 1686525, 11 pages
https://doi.org/10.1155/2017/1686525
Research Article

MicroPET/CT Imaging of AXL Downregulation by HSP90 Inhibition in Triple-Negative Breast Cancer

1Department of Cancer Systems Imaging, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
2Department of Radiology, The 1st Affiliated Hospital of Anhui Medical University, Hefei, Anhui, China
3Department of Systems Biology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

Correspondence should be addressed to Yongqiang Yu; moc.361.piv@gnaiqgnoyuy.rjc, Shiaw-Yih Lin; gro.nosrednadm@nilys, and Chun Li; gro.nosrednadm@ilc

Received 7 February 2017; Accepted 2 April 2017; Published 14 May 2017

Academic Editor: Kai Yang

Copyright © 2017 Wanqin Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. Weigelt, J. L. Peterse, and L. J. van't Veer, “Breast cancer metastasis: markers and models,” Nature Reviews Cancer, vol. 5, no. 8, pp. 591–602, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. J. P. Their, “Epithelial-mesenchymal transitions in tumor progression,” Nature Reviews Cancer, vol. 2, no. 6, pp. 442–454, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Thomson, F. Petti, I. Sujka-Kwok et al., “A systems view of epithelial-mesenchymal transition signaling states,” Clinical and Experimental Metastasis, vol. 28, no. 2, pp. 137–155, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. B. G. Haffty, Q. Yang, M. Reiss et al., “Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer,” Journal of Clinical Oncology, vol. 24, no. 36, pp. 5652–5657, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. B. D. Lehmann, J. A. Bauer, X. Chen et al., “Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies,” Journal of Clinical Investigation, vol. 121, no. 7, pp. 2750–2767, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. S. H. Myers, V. G. Brunton, and A. Unciti-Broceta, “AXL inhibitors in cancer: a medicinal chemistry perspective,” Journal of Medicinal Chemistry, vol. 59, no. 8, pp. 3593–3608, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. M. K. Asiedu, F. D. Beauchamp-Perez, J. N. Ingle, M. D. Behrens, D. C. Radisky, and K. L. Knutson, “AXL induces epithelial-to-mesenchymal transition and regulates the function of breast cancer stem cells,” Oncogene, vol. 33, no. 10, pp. 1316–1324, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. D. N. Debruyne, N. Bhatnagar, B. Sharma et al., “ALK inhibitor resistance in ALKF1174L-driven neuroblastoma is associated with AXL activation and induction of EMT,” Oncogene, vol. 35, no. 28, pp. 3681–3691, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. X. Wu, X. Liu, S. Koul, C. Y. Lee, Z. Zhang, and B. Halmos, “AXL kinase as a novel target for cancer therapy,” Oncotarget, vol. 5, no. 20, pp. 9546–9563, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. Y.-S. Shieh, C.-Y. Lai, Y.-R. Kao et al., “Expression of Axl in lung adenocarcinoma and correlation with tumor progression,” Neoplasia, vol. 7, no. 12, pp. 1058–1064, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Gjerdrum, C. Tiron, T. Høiby et al., “Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 3, pp. 1124–1129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. J. B. Koorstra, C. A. Karikari, G. Feldmann et al., “The Axl receptor tyrosine kinase confers an adverse prognostic influence in pancreatic cancer and represents a new therapeutic target,” Cancer Biology & Therapy, vol. 8, no. 7, pp. 618–626, 2009. View at Publisher · View at Google Scholar
  13. T. M. Brand, M. Iida, A. P. Stein et al., “AXL mediates resistance to cetuximab therapy,” Cancer Research, vol. 74, no. 18, pp. 5152–5164, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Postel-Vinay and A. Ashworth, “AXL and acquired resistance to EGFR inhibitors,” Nature Genetics, vol. 44, no. 8, pp. 835-836, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. A. S. Meyer, M. A. Miller, F. B. Gertler, and D. A. Lauffenburger, “The receptor AXL diversifies EGFR signaling and limits the response to EGFR-targeted inhibitors in triple-negative breast cancer cells,” Science Signaling, vol. 6, no. 287, article ra66, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Y. Bae, J.-Y. Hong, H.-J. Lee, H. J. Park, and S. K. Lee, “Targeting the degradation of AXL receptor tyrosine kinase to overcome resistance in gefitinib-resistant non-small cell lung cancer,” Oncotarget, vol. 6, no. 12, pp. 10146–10160, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Li, X. Ye, C. Tan et al., “Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis,” Oncogene, vol. 28, no. 39, pp. 3442–3455, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. E. B. Rankin, K. C. Fuh, T. E. Taylor et al., “AXL is an essential factor and therapeutic target for metastatic ovarian cancer,” Cancer Research, vol. 70, no. 19, pp. 7570–7579, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Sheridan, “First Axl inhibitor enters clinical trials,” Nature Biotechnology, vol. 31, no. 9, pp. 775-776, 2013. View at Google Scholar · View at Scopus
  20. X. Wu, M. S. Zahari, B. Ma et al., “Global phosphotyrosine survey in triple-negative breast cancer reveals activation of multiple tyrosine kinase signaling pathways,” Oncotarget, vol. 6, no. 30, pp. 29143–29160, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Jiao, W. Ou, F. Meng, H. Zhou, and A. Wang, “Targeting HSP90 in ovarian cancers with multiple receptor tyrosine kinase coactivation,” Molecular Cancer, vol. 10, article 125, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Khandelwal, V. M. Crowley, and B. S. J. Blagg, “Natural product inspired N-terminal Hsp90 inhibitors: from bench to bedside?” Medicinal Research Reviews, vol. 36, no. 1, pp. 92–118, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. Wu, X. Zhang, Z. Xiong et al., “microPET imaging of glioma integrin avb3 expression using (64)Cu-labeled tetrameric RGD peptide,” Journal of Nuclear Medicine, vol. 46, no. 10, pp. 1707–1718, 2005. View at Google Scholar
  24. J. Crown, J. O'Shaughnessy, and G. Gullo, “Emerging targeted therapies in triple-negative breast cancer,” Annals of Oncology, vol. 23, no. 6, pp. vi56–vi65, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Nimmagadda, M. Pullambhatla, A. Lisok, C. Hu, A. Maitra, and M. G. Pomper, “Imaging Axl expression in pancreatic and prostate cancer xenografts,” Biochemical and Biophysical Research Communications, vol. 443, no. 2, pp. 635–640, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Li, S. Liu, R. Liu et al., “Axl-targeted cancer imaging with humanized antibody h173,” Molecular Imaging and Biology, vol. 16, no. 4, pp. 511–518, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Liu, D. Li, J. Guo et al., “Design, synthesis, and validation of Axl-targeted monoclonal antibody probe for microPET imaging in human lung cancer xenograft,” Molecular Pharmaceutics, vol. 11, no. 11, pp. 3974–3979, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. C. J. Anderson and R. Ferdani, “Copper-64 radiopharmaceuticals for PET imaging of cancer: advances in preclinical and clinical research,” Cancer Biotherapy and Radiopharmaceuticals, vol. 24, no. 4, pp. 379–393, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. M. S. Cooper, M. T. Ma, K. Sunassee et al., “Comparison of 64cu-complexing bifunctional chelators for radioimmunoconjugation: labeling efficiency, specific activity, and in vitro/in vivo stability,” Bioconjugate Chemistry, vol. 23, no. 5, pp. 1029–1039, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Zhou, J. Zhao, M. Tian et al., “Radio-photothermal therapy mediated by a single compartment nanoplatform depletes tumor initiating cells and reduces lung metastasis in the orthotopic 4T1 breast tumor model,” Nanoscale, vol. 7, no. 46, pp. 19438–19447, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. G. P. Krishnamoorthy, T. Guida, L. Alfano et al., “Molecular mechanism of 17-allylamino-17-demethoxygeldanamycin (17-AAG)-induced AXL receptor tyrosine kinase degradation,” Journal of Biological Chemistry, vol. 288, no. 24, pp. 17481–17494, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Li, T. Zhang, S. J. Schwartz, and D. Sun, “New developments in Hsp90 inhibitors as anti-cancer therapeutics: Mechanisms, clinical perspective and more potential,” Drug Resistance Updates, vol. 12, no. 1-2, pp. 17–27, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. P. M. Smith-Jones, D. B. Solit, T. Akhurst, F. Afroze, N. Rosen, and S. M. Larson, “Imaging the pharmacodynamics of HER2 degradation in response to Hsp90 inhibitors,” Nature Biotechnology, vol. 22, no. 6, pp. 701–706, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Spiegelberg, A. C. Mortensen, R. K. Selvaraju, O. Eriksson, B. Stenerlöw, and M. Nestor, “Molecular imaging of EGFR and CD44v6 for prediction and response monitoring of HSP90 inhibition in an in vivo squamous cell carcinoma model,” European Journal of Nuclear Medicine and Molecular Imaging, vol. 43, no. 5, pp. 974–982, 2016. View at Publisher · View at Google Scholar · View at Scopus
  35. Z. Cai and C. J. Anderson, “Chelators for copper radionuclides in positron emission tomography radiopharmaceuticals,” Journal of Labelled Compounds and Radiopharmaceuticals, vol. 57, no. 4, pp. 224–230, 2014. View at Publisher · View at Google Scholar · View at Scopus