Table of Contents Author Guidelines Submit a Manuscript
Bone Marrow Research
Volume 2014, Article ID 405920, 12 pages
http://dx.doi.org/10.1155/2014/405920
Review Article

Molecular Regulation of Bone Marrow Metastasis in Prostate and Breast Cancer

1Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz 61357-15794, Iran
2Health Research Institute, Research Center of Thalassemia & Hemoglobinopathy, Ahvaz Jundishapur University of Medical Sciences, Ahvaz 61357-15794, Iran
3Division of Pharmacology and Pathophysiology, Utrecht Institute for Pharmaceutical Sciences, Faculty of Sciences, Utrecht University, 80082 Utrecht, The Netherlands
4Clinical Tuberculosis and Epidemiology Research Center, National Research and Institute of Tuberculosis and Lung Diseases (NRITLD), Shahid Beheshti University of Medical Sciences, 19575/154 Tehran, Iran
5Cell and Molecular Biology Group, Airways Disease Section, National Heart and Lung Institute, Imperial College London, Dovehouse Street, London SW7 2AZ, UK
6Department of Biochemistry and Hematology, Faculty of Medicine, Semnan University of Medical Sciences, Semnan 35131-38111, Iran

Received 11 February 2014; Revised 9 June 2014; Accepted 11 June 2014; Published 23 July 2014

Academic Editor: Peter J. Quesenberry

Copyright © 2014 Fakher Rahim 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. M. F. Leber and T. Efferth, “Molecular principles of cancer invasion and metastasis: review,” International Journal of Oncology, vol. 34, no. 4, pp. 881–895, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. L. J. Suva, C. Washam, R. W. Nicholas, and R. J. Griffin, “Bone metastasis: mechanisms and therapeutic opportunities,” Nature Reviews. Endocrinology, vol. 7, no. 4, pp. 208–218, 2011. View at Publisher · View at Google Scholar
  3. J. P. Sleeman, “The metastatic niche and stromal progression,” Cancer and Metastasis Reviews, vol. 31, no. 3-4, pp. 429–440, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Azizidoost, S. Babashah, F. Rahim, M. Shahjahani, and N. Saki, “Bone marrow neoplastic niche in leukemia,” Hematology, vol. 19, no. 4, pp. 232–238, 2013. View at Google Scholar
  5. N. Saki, S. Abroun, M. F. Hagh, and F. Asgharei, “Neoplastic bone marrow niche: hematopoietic and mesenchymal stem cells,” Cell Journal, vol. 13, no. 3, pp. 131–136, 2011. View at Google Scholar · View at Scopus
  6. A. C. Chiang and J. Massague, “Molecular basis of metastasis,” The New England Journal of Medicine, vol. 359, no. 26, pp. 2814–2823, 2008. View at Publisher · View at Google Scholar
  7. G. P. Gupta and J. Massague, “Cancer metastasis: building a framework,” Cell, vol. 127, no. 4, pp. 679–95, 2006. View at Google Scholar
  8. J. E. Compston, “Bone marrow and bone: A functional unit,” Journal of Endocrinology, vol. 173, no. 3, pp. 387–394, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Yoneda and T. Hiraga, “Crosstalk between cancer cells and bone microenvironment in bone metastasis,” Biochemical and Biophysical Research Communications, vol. 328, no. 3, pp. 679–687, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. T. A. Guise, “The vicious cycle of bone metastases,” Journal of Musculoskeletal and Neuronal Interactions, vol. 2, no. 6, pp. 570–572, 2002. View at Google Scholar · View at Scopus
  11. A. A. N. Rose and P. M. Siegel, “Breast cancer-derived factors facilitate osteolytic bone metastasis,” Bulletin du Cancer, vol. 93, no. 9, pp. 931–943, 2006. View at Google Scholar · View at Scopus
  12. T. Shimo, S. Kubota, N. Yoshioka et al., “Pathogenic role of connective tissue growth factor (CTGF/CCN2) in osteolytic metastasis of breast cancer,” Journal of Bone and Mineral Research, vol. 21, no. 7, pp. 1045–1059, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. J. J. Yin, K. Selander, J. M. Chirgwin et al., “TGF-β signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development,” Journal of Clinical Investigation, vol. 103, no. 2, pp. 197–206, 1999. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Mori, B. Le Goff, C. Charrier, S. Battaglia, D. Heymann, and F. Rédini, “DU145 human prostate cancer cells express functional receptor activator of NFκB: new insights in the prostate cancer bone metastasis process,” Bone, vol. 40, no. 4, pp. 981–990, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. G. D. Roodman, “Mechanisms of bone metastasis,” The New England Journal of Medicine, vol. 350, no. 16, pp. 1655–1664, 2004. View at Publisher · View at Google Scholar
  16. N. Sethi and Y. Kang, “Dysregulation of developmental pathways in bone metastasis,” Bone, vol. 48, no. 1, pp. 16–22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Ara and Y. A. Declerck, “Interleukin-6 in bone metastasis and cancer progression,” European Journal of Cancer, vol. 46, no. 7, pp. 1223–1231, 2010. View at Google Scholar
  18. Y. Kang, W. He, S. Tulley et al., “Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 39, pp. 13909–13914, 2005. View at Publisher · View at Google Scholar
  19. Y. Katsuno, A. Hanyu, H. Kanda et al., “Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway,” Oncogene, vol. 27, no. 49, pp. 6322–6333, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. K. Conley-LaComb, A. Saliganan, P. Kandagatla, Y. Q. Chen, M. L. Cher, and S. R. Chinni, “PTEN loss mediated Akt activation promotes prostate tumor growth and metastasis via CXCL12/CXCR4 signaling,” Molecular Cancer, vol. 12, no. 1, article 85, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. X. H. Zhang, Q. Wang, W. Gerald et al., “Latent bone metastasis in breast cancer tied to Src-dependent survival signals,” Cancer Cell, vol. 16, no. 1, pp. 67–78, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Irmisch and J. Huelsken, “Metastasis: new insights into organ-specific extravasation and metastatic niches,” Experimental Cell Research, vol. 319, no. 11, pp. 1604–1610, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. Q. Chen and J. Massagué, “Molecular pathways: VCAM-1 as a potential therapeutic target in metastasis,” Clinical Cancer Research, vol. 18, no. 20, pp. 5520–5525, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. X. Lu, E. Mu, Y. Wei et al., “VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging α4β1-positive osteoclast progenitors,” Cancer Cell, vol. 20, no. 6, pp. 701–714, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Pécheur, O. Peyruchaud, C. Serre et al., “Integrin alpha(v)beta3 expression confers on tumor cells a greater propensity to metastasize to bone,” The FASEB Journal, vol. 16, no. 10, pp. 1266–1268, 2002. View at Google Scholar · View at Scopus
  26. M. Wobus, R. Rangwala, I. Sheyn et al., “CD44 associates with EGFR and erbB2 in metastasizing mammary carcinoma cells,” Applied Immunohistochemistry and Molecular Morphology, vol. 10, no. 1, pp. 34–39, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Sethi, X. Dai, C. G. Winter, and Y. Kang, “Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells,” Cancer Cell, vol. 19, no. 2, pp. 192–205, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Valastyan and R. A. Weinberg, “Tumor metastasis: molecular insights and evolving paradigms,” Cell, vol. 147, no. 2, pp. 275–292, 2011. View at Publisher · View at Google Scholar
  29. N. Sethi and Y. Kang, “Notch signaling: mediator and therapeutic target of bone metastasis,” BoneKEy Reports, vol. 1, article 3, 2012. View at Google Scholar
  30. D. Mendoza-Villanueva, L. Zeef, and P. Shore, “Metastatic breast cancer cells inhibit osteoblast differentiation through the Runx2/CBFβ-dependent expression of the Wnt antagonist, sclerostin,” Breast Cancer Research, vol. 13, no. 5, article R106, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Bu, W. Lu, C. C. Liu et al., “Breast cancer-derived Dickkopf1 inhibits osteoblast differentiation and osteoprotegerin expression: Implication for breast cancer osteolytic bone metastases,” International Journal of Cancer, vol. 123, no. 5, pp. 1034–1042, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Yagiz and S. R. Rittling, “Both cell-surface and secreted CSF-1 expressed by tumor cells metastatic to bone can contribute to osteoclast activation,” Experimental Cell Research, vol. 315, no. 14, pp. 2442–2452, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Singh, D. D. Joshi, M. Hameed et al., “Increased expression of preprotachykinin-I and neurokinin receptors in human breast cancer cells: implications for bone marrow metastasis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 1, pp. 388–393, 2000. View at Google Scholar
  34. G. A. Clines, K. S. Mohammad, Y. Bao, O. W. Stephens, L. J. Suva, and J. D. Shaughnessy Jr., “Dickkopf homolog 1 mediates endothelin-1-stimulated new bone formation,” Molecular Endocrinology, vol. 21, no. 2, pp. 486–498, 2007. View at Google Scholar
  35. D. A. Glass II, P. Bialek, J. D. Ahn et al., “Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation,” Developmental Cell, vol. 8, no. 5, pp. 751–764, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. L. G. Schuettpelz and D. C. Link, “Niche competition and cancer metastasis to bone,” The Journal of Clinical Investigation, vol. 121, no. 4, pp. 1253–1255, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Jacob, M. Webber, D. Benayahu, and H. K. Kleinman, “Osteonectin promotes prostate cancer cell migration and invasion: a possible mechanism for metastasis to bone,” Cancer Research, vol. 59, no. 17, pp. 4453–4457, 1999. View at Google Scholar · View at Scopus
  38. N. Chen, X. Ye, K. Chu et al., “A secreted isoform of ErbB3 promotes osteonectin expression in bone and enhances the invasiveness of prostate cancer cells,” Cancer Research, vol. 67, no. 14, pp. 6544–6548, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. S. De, J. Chen, N. V. Narizhneva et al., “Molecular pathway for cancer metastasis to bone,” The Journal of Biological Chemistry, vol. 278, no. 40, pp. 39044–39050, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. S. M. Zunich, T. Douglas, M. Valdovinos et al., “Paracrine sonic hedgehog signalling by prostate cancer cells induces osteoblast differentiation,” Molecular Cancer, vol. 8, article 12, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. S. M. Zunich, M. Valdovinos, T. Douglas, D. Walterhouse, P. Iannaccone, and M. L. G. Lamm, “Osteoblast-secreted collagen upregulates paracrine Sonic hedgehog signaling by prostate cancer cells and enhances osteoblast differentiation,” Molecular Cancer, vol. 11, article 30, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. J. K. Kim, Y. Jung, J. Wang et al., “TBK1 regulates prostate cancer dormancy through mTOR inhibition,” Neoplasia, vol. 15, no. 9, pp. 1064–1074, 2013. View at Publisher · View at Google Scholar
  43. S. F. Shariat, C. G. Roehrborn, J. D. McConnell et al., “Association of the circulating levels of the urokinase system of plasminogen activation with the presence of prostate cancer and invasion, progression, and metastasis,” Journal of Clinical Oncology, vol. 25, no. 4, pp. 349–355, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Miyake, I. Hara, K. Yamanaka, K. Gohji, S. Arakawa, and S. Kamidono, “Elevation of serum levels of urokinase-type plasminogen activator and its receptor is associated with disease progression and prognosis in patients with prostate cancer,” Prostate, vol. 39, no. 2, pp. 123–129, 1999. View at Google Scholar
  45. D. Cai, J. Cao, Z. Li et al., “Up-regulation of bone marrow stromal protein 2 (BST2) in breast cancer with bone metastasis,” BMC Cancer, vol. 9, article 102, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Abroun, N. Saki, R. Fakher, and F. Asghari, “Biology and bioinformatics of myeloma cell,” Laboratory Hematology, vol. 18, no. 4, pp. 30–41, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. B. K. Park, H. Zhang, Q. Zeng et al., “NF-κB in breast cancer cells promotes osteolytic bone metastasis by inducing osteoclastogenesis via GM-CSF,” Nature Medicine, vol. 13, no. 1, pp. 62–69, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Yang, K. Fizazi, S. Peleg et al., “Prostate cancer cells induce osteoblast differentiation through a Cbfa1-dependent pathway,” Cancer Research, vol. 61, no. 14, pp. 5652–5659, 2001. View at Google Scholar · View at Scopus
  49. C. L. Hall, A. Bafico, J. Dai, S. A. Aaronson, and E. T. Keller, “Prostate cancer cells promote osteoblastic bone metastases through Wnts,” Cancer Research, vol. 65, no. 17, pp. 7554–7560, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. E. Zhao, L. Wang, J. Dai et al., “Regulatory T cells in the bone marrow microenvironment in patients with prostate cancer,” Oncoimmunology, vol. 1, no. 2, pp. 152–161, 2012. View at Publisher · View at Google Scholar
  51. N. Rucci and A. Angelucci, “Prostate cancer and bone: the elective affinities,” BioMed Research International, vol. 2014, Article ID 167035, 14 pages, 2014. View at Publisher · View at Google Scholar
  52. S. H. Lin, Y. C. Lee, M. B. Choueiri et al., “Soluble ErbB3 levels in bone marrow and plasma of men with prostate cancer,” Clinical Cancer Research, vol. 14, no. 12, pp. 3729–3736, 2008. View at Google Scholar
  53. P. Li, Y. Gao, Z. Ji et al., “Role of urokinase plasminogen activator and its receptor in metastasis and invasion of neuroblastoma,” Journal of Pediatric Surgery, vol. 39, no. 10, pp. 1512–1519, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. X. Ye, Y. C. Lee, M. Choueiri et al., “Aberrant expression of katanin p60 in prostate cancer bone metastasis,” Prostate, vol. 72, no. 3, pp. 291–300, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. R. Jin, J. A. Sterling, J. R. Edwards et al., “Activation of NF-kappa B signaling promotes growth of prostate cancer cells in bone,” PLoS ONE, vol. 8, no. 4, Article ID e60983, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Descot and T. Oskarsson, “The molecular composition of the metastatic niche,” Experimental Cell Research, vol. 319, no. 11, pp. 1673–1686, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. S. M. Frisch and R. A. Screaton, “Anoikis mechanisms,” Current Opinion in Cell Biology, vol. 13, no. 5, pp. 555–562, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Labelle, S. Begum, and R. O. Hynes, “Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis,” Cancer Cell, vol. 20, no. 5, pp. 576–590, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Boucharaba, C. Serre, S. Grès et al., “Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer,” Journal of Clinical Investigation, vol. 114, no. 12, pp. 1714–1725, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. B. Psaila, D. Lyden, and I. Roberts, “Megakaryocytes, malignancy and bone marrow vascular niches,” Journal of Thrombosis and Haemostasis, vol. 10, no. 2, pp. 177–188, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. F. Takeshita, L. Patrawala, M. Osaki et al., “Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes,” Molecular Therapy, vol. 18, no. 1, pp. 181–187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. H. L. Zhang, X. J. Qin, D. L. Cao et al., “An elevated serum miR-141 level in patients with bone-metastatic prostate cancer is correlated with more bone lesions,” Asian Journal of Andrology, vol. 15, no. 2, pp. 231–235, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. X. Peng, W. Guo, T. Liu et al., “Identification of miRs-143 and -145 that is associated with bone metastasis of prostate cancer and involved in the regulation of EMT,” PLoS ONE, vol. 6, no. 5, Article ID e20341, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Huang, W. Guo, Y. Tang, D. Ren, X. Zou, and X. Peng, “miR-143 and miR-145 inhibit stem cell characteristics of PC-3 prostate cancer cells,” Oncology Reports, vol. 28, no. 5, pp. 1831–1837, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. W. Guo, D. Ren, X. Chen et al., “HEF1 promotes epithelial mesenchymal transition and bone invasion in prostate cancer under the regulation of microRNA-145,” Journal of Cellular Biochemistry, vol. 114, no. 7, pp. 1606–1615, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Saini, S. Majid, S. Yamamura et al., “Regulatory role of mir-203 in prostate cancer progression and metastasis,” Clinical Cancer Research, vol. 17, no. 16, pp. 5287–5298, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Q. Hassan, Y. Maeda, H. Taipaleenmaki et al., “miR-218 directs a Wnt signaling circuit to promote differentiation of osteoblasts and osteomimicry of metastatic cancer cells,” The Journal of Biological Chemistry, vol. 287, no. 50, pp. 42084–42092, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. L. Huang, T. Dai, X. Lin et al., “MicroRNA-224 targets RKIP to control cell invasion and expression of metastasis genes in human breast cancer cells,” Biochemical and Biophysical Research Communications, vol. 425, no. 2, pp. 127–133, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Baranwal and S. K. Alahari, “miRNA control of tumor cell invasion and metastasis,” International Journal of Cancer, vol. 126, no. 6, pp. 1283–1290, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. L. Ma and R. A. Weinberg, “Micromanagers of malignancy: role of microRNAs in regulating metastasis,” Trends in Genetics, vol. 24, no. 9, pp. 448–456, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. B. Ell, L. Mercatali, T. Ibrahim et al., “Tumor-induced osteoclast miRNA changes as regulators and biomarkers of osteolytic bone metastasis,” Cancer Cell, vol. 24, no. 4, pp. 542–556, 2013. View at Google Scholar
  72. N. Saki, S. Abroun, S. Hajizamani, F. Rahim, and M. Shahjahani, “Association of chromosomal translocation and miRNA expression with the pathogenesis of multiple myeloma,” Cell Journal, vol. 16, no. 2, 2013. View at Google Scholar
  73. J. C. Brase, M. Johannes, T. Schlomm et al., “Circulating miRNAs are correlated with tumor progression in prostate cancer,” International Journal of Cancer, vol. 128, no. 3, pp. 608–616, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. N. Pencheva and S. F. Tavazoie, “Control of metastatic progression by microRNA regulatory networks,” Nature Cell Biology, vol. 15, no. 6, pp. 546–554, 2013. View at Google Scholar
  75. A. D. Pyle, P. J. Donovan, and L. F. Lock, “Chipping away ‘stemness’,” Genome Biology, vol. 5, no. 8, article 235, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Vimalraj, P. J. Miranda, B. Ramyakrishna, and N. Selvamurugan, “Regulation of breast cancer and bone metastasis by microRNAs,” Disease Markers, vol. 35, no. 5, pp. 369–387, 2013. View at Google Scholar
  77. C. Lopez-Camarillo, L. A. Marchat, E. Arechaga-Ocampo et al., “MetastamiRs: non-coding microRNAs driving cancer invasion and metastasis,” International Journal of Molecular Sciences, vol. 13, no. 2, pp. 1347–1379, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. Z. Fu, P. C. Smith, L. Zhang et al., “Effects of Raf kinase inhibitor protein expression on suppression of prostate cancer metastasis,” Journal of the National Cancer Institute, vol. 95, no. 12, pp. 878–889, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. Z. Fu, Y. Kitagawa, R. Shen et al., “Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer,” Prostate, vol. 66, no. 3, pp. 248–256, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. A. Ben Jemaa, Y. Bouraoui, S. Sallami, Y. Nouira, and R. Oueslati, “A comparison of the biological features of prostate cancer with (PSA+, PSMA+) profile according to RKIP,” BioMed Research International, vol. 2013, Article ID 409179, 7 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. E. T. Keller, Z. Fu, and M. Brennan, “The biology of a prostate cancer metastasis suppressor protein: raf kinase inhibitor protein,” Journal of Cellular Biochemistry, vol. 94, no. 2, pp. 273–278, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Dangi-Garimella, J. Yun, E. M. Eves et al., “Raf kinase inhibitory protein suppresses a metastasis signalling cascade involving LIN28 and let-7,” The EMBO Journal, vol. 28, no. 4, pp. 347–358, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. E. Bevilacqua, C. A. Frankenberger, and M. R. Rosner, “RKIP suppresses breast cancer metastasis to the bone by regulating stroma-associated genes,” International Journal of Breast Cancer, vol. 2012, Article ID 124704, 5 pages, 2012. View at Publisher · View at Google Scholar
  84. S. M. A. Rad, M. S. Bavarsad, E. Arefian, K. Jaseb, M. Shahjahani, and N. Saki, “The role of microRNAs in stemness of cancer stem cells,” Oncology Reviews, vol. 7, no. 1, article e8, 2013. View at Publisher · View at Google Scholar
  85. S. Yousuf, M. Duan, E. L. Moen, S. Cross-Knorr, K. Brilliant, and B. Bonavida, “Raf Kinase Inhibitor Protein (RKIP) blocks signal transducer and activator of transcription 3 (STAT3) activation in breast and prostate cancer,” PLoS One, vol. 9, no. 3, article e92478, 2014. View at Google Scholar
  86. B. Bonavida, S. Baritaki, S. Huerta-Yepez, M. I. Vega, D. Chatterjee, and K. Yeung, “Novel therapeutic applications of nitric oxide donors in cancer: roles in chemo- and immunosensitization to apoptosis and inhibition of metastases,” Nitric Oxide: Biology and Chemistry, vol. 19, no. 2, pp. 152–157, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Baritaki, A. Katsman, D. Chatterjee, K. C. Yeung, D. A. Spandidos, and B. Bonavida, “Regulation of tumor cell sensitivity to TRAIL-induced apoptosis by the metastatic suppressor raf kinase inhibitor protein via Yin Yang 1 inhibition and death receptor 5 up-regulation,” Journal of Immunology, vol. 179, no. 8, pp. 5441–5453, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. D. Chatterjee, Y. Bai, Z. Wang et al., “RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis,” The Journal of Biological Chemistry, vol. 279, no. 17, pp. 17515–17523, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. F.-L. Zhaoa, G.-D. Hua, X.-F. Wang, X.-H. Zhang, Y.-K. Zhang, and Z.-S. Yu, “Serum overexpression of microRNA-10b in patients with bone metastatic primary breast cancer,” The Journal of International Medical Research, vol. 40, no. 3, pp. 859–866, 2012. View at Publisher · View at Google Scholar · View at Scopus
  90. T. A. Guise, “Breaking down bone: new insight into site-specific mechanisms of breast cancer osteolysis mediated by metalloproteinases,” Genes and Development, vol. 23, no. 18, pp. 2117–2123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. L. Wan, K. Pantel, and Y. Kang, “Tumor metastasis: moving new biological insights into the clinic,” Nature Medicine, vol. 19, no. 11, pp. 1450–1464, 2013. View at Google Scholar
  92. B. I. Koh and Y. Kang, “The pro-metastatic role of bone marrow-derived cells: a focus on MSCs and regulatory T cells,” EMBO Reports, vol. 13, no. 5, pp. 412–422, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. R. R. Langley and I. J. Fidler, “The seed and soil hypothesis revisited—the role of tumor-stroma interactions in metastasis to different organs,” International Journal of Cancer, vol. 128, no. 11, pp. 2527–2535, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. N. Mehra, M. Penning, J. Maas et al., “Progenitor marker CD133 mRNA is elevated in peripheral blood of cancer patients with bone metastases,” Clinical Cancer Research, vol. 12, no. 16, pp. 4859–4866, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. J. E. Hartwich, W. S. Orr, C. Y. Ng et al., “Rapamycin increases neuroblastoma xenograft and host stromal derived osteoprotegerin inhibiting osteolytic bone disease in a bone metastasis model,” Journal of Pediatric Surgery, vol. 48, no. 1, pp. 47–55, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. N. Otmani and M. Khattab, “Metastatic neuroblastoma to the mandible in a 3-year-old boy: a case report,” Medicina Oral, Patología Oral y Cirugía Bucal, vol. 12, no. 3, pp. E201–E204, 2007. View at Google Scholar · View at Scopus
  97. M. Ma, J. Y. Ye, R. Deng, C. M. Dee, and G. C. Chan, “Mesenchymal stromal cells may enhance metastasis of neuroblastoma via SDF-1/CXCR4 and SDF-1/CXCR7 signaling,” Cancer Letters, vol. 312, no. 1, pp. 1–10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. T. Ara and Y. A. DeClerck, “Mechanisms of invasion and metastasis in human neuroblastoma,” Cancer and Metastasis Reviews, vol. 25, no. 4, pp. 645–657, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. Y. Fukaya, H. Shimada, L. C. Wang, E. Zandi, and Y. A. DeClerck, “Identification of galectin-3-binding protein as a factor secreted by tumor cells that stimulates interleukin-6 expression in the bone marrow stroma,” The Journal of Biological Chemistry, vol. 283, no. 27, pp. 18573–18581, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Wen, H. Wang, X. Zhang et al., “Cytokine-like 1 is involved in the growth and metastasis of neuroblastoma cells,” International Journal of Oncology, vol. 41, no. 4, pp. 1419–1424, 2012. View at Publisher · View at Google Scholar · View at Scopus