Table of Contents Author Guidelines Submit a Manuscript
Journal of Oncology
Volume 2012 (2012), Article ID 782020, 15 pages
http://dx.doi.org/10.1155/2012/782020
Review Article

Targeting Angiogenesis for Controlling Neuroblastoma

1Department of Pathology, Microbiology, and Immunology, University of South Carolina School of Medicine, Columbia, SC 29209, USA
2Department of Neurosciences, Medical University of South Carolina, Charleston, SC 29425, USA

Received 6 May 2011; Accepted 3 June 2011

Academic Editor: Arkadiusz Dudek

Copyright © 2012 Subhasree Roy Choudhury 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. E. Hiyama, T. Iehara, T. Sugimoto et al., “Effectiveness of screening for neuroblastoma at 6 months of age: a retrospective population-based cohort study,” The Lancet, vol. 371, no. 9619, pp. 1173–1180, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Ogawa, J. Takita, M. Sanada, and Y. Hayashi, “Oncogenic mutations of ALK in neuroblastoma,” Cancer Science, vol. 102, no. 2, pp. 302–308, 2011. View at Google Scholar
  3. J. Rössler, Y. Monnet, F. Farace et al., “The selective VEGFR1-3 inhibitor axitinib (AG-013736) shows antitumor activity in human neuroblastoma xenografts,” International Journal of Cancer, vol. 128, no. 11, pp. 2748–2758, 2011. View at Google Scholar
  4. S. B. Fox, G. Gasparini, and A. L. Harris, “Angiogenesis: pathological, prognostic, and growth-factor pathways and their link to trial design and anticancer drugs,” Lancet Oncology, vol. 2, no. 5, pp. 278–289, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. I. M. Herman and F. Nussenbaum, “Tumor angiogenesis: insights and innovations,” Journal of Oncology, vol. 2010, Article ID 132641, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Oklu, T. G. Walker, S. Wicky, and R. Hesketh, “Angiogenesis and current antiangiogenic strategies for the treatment of cancer,” Journal of Vascular and Interventional Radiology, vol. 21, no. 12, pp. 1791–1805, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Lyons 3rd, C. T. Anthony, and E. A. Woltering, “The role of angiogenesis in neuroendocrine tumors,” Endocrinology and Metabolism Clinics of North America, vol. 39, no. 4, pp. 839–852, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Saharinen, M. Bry, and K. Alitalo, “How do angiopoietins Tie in with vascular endothelial growth factors?” Current Opinion in Hematology, vol. 17, no. 3, pp. 198–205, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. R. J. Kelly, C. Darnell, and O. Rixe, “Target inhibition in antiangiogenic therapy a wide spectrum of selectivity and specificity,” Cancer Journal, vol. 16, no. 6, pp. 635–642, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Beppu, J. Jaboine, M. S. Merchant, C. L. Mackall, and C. J. Thiele, “Effect of imatinib mesylate on neuroblastoma tumorigenesis and vascular endothelial growth factor expression,” Journal of the National Cancer Institute, vol. 96, no. 1, pp. 46–55, 2004. View at Google Scholar · View at Scopus
  11. M. Fakhari, D. Pullirsch, K. Paya, D. Abraham, R. Hofbauer, and S. Aharinejad, “Upregulation of vascular endothelial growth factor receptors is associated with advanced neuroblastoma,” Journal of Pediatric Surgery, vol. 37, no. 4, pp. 582–587, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. I. Langer, P. Vertongen, J. Perret, J. Fontaine, G. Atassi, and P. Robberecht, “Expression of vascular endothelial growth factor (VEGF) and VEGF receptors in human neuroblastomas,” Medical and Pediatric Oncology, vol. 34, no. 6, pp. 386–393, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. B. Das, H. Yeger, R. Tsuchida et al., “A hypoxia-driven vascular endothelial growth factor/Flt1 autocrine loop interacts with hypoxia-inducible factor-1α through mitogen-activated protein kinase/extracellular signal-regulated kinase 1/2 pathway in neuroblastoma,” Cancer Research, vol. 65, no. 16, pp. 7267–7275, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Ribatti, D. Marimpietri, F. Pastorino et al., “Angiogenesis in neuroblastoma,” Annals of the New York Academy of Sciences, vol. 1028, pp. 133–142, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Brignole, D. Marimpietri, F. Pastorino et al., “Effect of bortezomib on human neuroblastoma cell growth, apoptosis, and angiogenesis,” Journal of the National Cancer Institute, vol. 98, no. 16, pp. 1142–1157, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. J. B. Hamner, P. V. Dickson, T. L. Sims et al., “Bortezomib inhibits angiogenesis and reduces tumor burden in a murine model of neuroblastoma,” Surgery, vol. 142, no. 2, pp. 185–191, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Segerström, D. Fuchs, U. Bäckman, K. Holmquist, R. Christofferson, and F. Azarbayjani, “The anti-VEGF antibody bevacizumab potently reduces the growth rate of high-risk neuroblastoma xenografts,” Pediatric Research, vol. 60, no. 5, pp. 576–581, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Beaudry, M. Nilsson, M. Rioth et al., “Potent antitumor effects of ZD6474 on neuroblastoma via dual targeting of tumor cells and tumor endothelium,” Molecular Cancer Therapeutics, vol. 7, no. 2, pp. 418–424, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. E. S. Kim, A. Serur, J. Huang et al., “Potent VEGF blockade causes regression of coopted vessels in a model of neuroblastoma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 17, pp. 11399–11404, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Eggert, N. Ikegaki, J. Kwiatkowski, H. Zhao, G. M. Brodeur, and B. P. Himelstein, “High-level expression of angiogenic factors is associated with advanced tumor stage in human neuroblastomas,” Clinical Cancer Research, vol. 6, no. 5, pp. 1900–1908, 2000. View at Google Scholar · View at Scopus
  21. A. Shimada, J. Hirato, M. Kuroiwa et al., “Expression of KIT and PDGFR is associated with a good prognosis in neuroblastoma,” Pediatric Blood and Cancer, vol. 50, no. 2, pp. 213–217, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Funa and A. Åhgren, “Characterization of platelet-derived growth factor (PDGF) action on a mouse neuroblastoma cell line, NB41, by introduction of an antisense PDGF/β- receptor RNA,” Cell Growth and Differentiation, vol. 8, no. 8, pp. 861–869, 1997. View at Google Scholar · View at Scopus
  23. U. Bäckman and R. Christofferson, “The selective class III/V receptor tyrosine kinase inhibitor SU11657 inhibits tumor growth and angiogenesis in experimental neuroblastomas grown in mice,” Pediatric Research, vol. 57, no. 5 I, pp. 690–695, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. M. G. Cattaneo, G. Scita, and L. M. Vicentini, “Somatostatin inhibits PDGF-stimulated Ras activation in human neuroblastoma cells,” FEBS Letters, vol. 459, no. 1, pp. 64–68, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. P. S. Cohen, J. P. Chan, M. Lipkunskaya, J. L. Biedler, and R. C. Seeger, “Expression of stem cell factor and c-kit in human neuroblastoma,” Blood, vol. 84, no. 10, pp. 3465–3472, 1994. View at Google Scholar · View at Scopus
  26. F. Timeus, E. Ricotti, N. Crescenzio et al., “Flt-3 and its ligand are expressed in neural crest-derived tumors and promote survival and proliferation of their cell lines,” Laboratory Investigation, vol. 81, no. 7, pp. 1025–1037, 2001. View at Google Scholar · View at Scopus
  27. R. Vitali, V. Cesi, M. R. Nicotra et al., “c-Kit is preferentially expressed in MYCN-amplified neuroblastoma and its effect on cell proliferation is inhibited in vitro by STI-571,” International Journal of Cancer, vol. 106, no. 2, pp. 147–152, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Strippoli, G. P. Bagnara, L. Montanaro, F. Timeus, A. M. Ferreri, and P. Rocchi, “Retinoic acid modulates stem cell factor secretion by human neuroblastoma cell lines,” Anticancer Research, vol. 20, no. 6 B, pp. 4361–4366, 2000. View at Google Scholar · View at Scopus
  29. F. Timeus, N. Crescenzio, P. Valle et al., “Stem cell factor suppresses apoptosis in neuroblastoma cell lines,” Experimental Hematology, vol. 25, no. 12, pp. 1253–1260, 1997. View at Google Scholar · View at Scopus
  30. T. Ara, M. Fukuzawa, T. Kusafuka et al., “Immunohistochemical expression of MMP-2, MMP-9, and TIMP-2 in neuroblastoma: association with tumor progression and clinical outcome,” Journal of Pediatric Surgery, vol. 33, no. 8, pp. 1272–1278, 1998. View at Google Scholar · View at Scopus
  31. C. F. Chantrain, H. Shimada, S. Jodele et al., “Stromal matrix metalloproteinase-9 regulates the vascular architecture in neuroblastoma by promoting pericyte recruitment,” Cancer Research, vol. 64, no. 5, pp. 1675–1686, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. F. Pastorino, M. Loi, P. Sapra et al., “Tumor regression and curability of preclinical neuroblastoma models by PEGylated SN38 (EZN-2208), a novel topoisomerase I inhibitor,” Clinical Cancer Research, vol. 16, no. 19, pp. 4809–4821, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Sugiura, H. Shimada, R. C. Seeger, W. E. Laug, and Y. A. DeClerck, “Matrix metalloproteinases-2 and -9 are expressed in human neuroblastoma: contribution of stromal cells to their production and correlation with metastasis,” Cancer Research, vol. 58, no. 10, pp. 2209–2216, 1998. View at Google Scholar · View at Scopus
  34. S. Joshi, R. S. Guleria, J. Pan, D. DiPette, and U. S. Singh, “Heterogeneity in retinoic acid signaling in neuroblastomas: role of matrix metalloproteinases in retinoic acid-induced differentiation,” Biochimica et Biophysica Acta, vol. 1772, no. 9, pp. 1093–1102, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Jodele, C. F. Chantrain, L. Blavier et al., “The contribution of bone marrow-derived cells to the tumor vasculature in neuroblastoma is matrix metalloproteinaae-9 dependent,” Cancer Research, vol. 65, no. 8, pp. 3200–3208, 2005. View at Google Scholar · View at Scopus
  36. D. Noujaim, C. M. Van Golen, K. L. Van Golen, A. Grauman, and E. L. Feldman, “N-Myc and Bcl-2 coexpression induces MMP-2 secretion and activation in human neuroblastoma cells,” Oncogene, vol. 21, no. 29, pp. 4549–4557, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Shusterman and J. M. Maris, “Prospects for therapeutic inhibition of neuroblastoma angiogenesis,” Cancer Letters, vol. 228, no. 1-2, pp. 171–179, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. G. M. Brodeur, “Neuroblastoma: biological insights into a clinical enigma,” Nature Reviews Cancer, vol. 3, no. 3, pp. 203–216, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Cetinkaya, A. Hultquist, Y. Su et al., “Combined IFN-γ and retinoic acid treatment targets the N-Myc/Max/Mad1 network resulting in repression of N-Myc target genes in MYCN-amplified neuroblastoma cells,” Molecular Cancer Therapeutics, vol. 6, no. 10, pp. 2634–2641, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Gross, K. Balmas, and C. B. Brognara, “Absence of functional CD44 hyaluronan receptor on human NMYC-amplified neuroblastoma cells,” Cancer Research, vol. 57, no. 7, pp. 1387–1393, 1997. View at Google Scholar · View at Scopus
  41. J. Kang, P. G. Rychahou, T. A. Ishola, J. M. Mourot, B. M. Evers, and D. H. Chung, “N-myc is a novel regulator of PI3K-mediated VEGF expression in neuroblastoma,” Oncogene, vol. 27, no. 28, pp. 3999–4007, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Pession, R. Tonelli, R. Fronza et al., “Targeted inhibition of NMYC by peptide nucleic acid in N-myc amplified human neuroblastoma cells: cell-cycle inhibition with induction of neuronal cell differentiation and apoptosis,” International Journal of Oncology, vol. 24, no. 2, pp. 265–272, 2004. View at Google Scholar · View at Scopus
  43. J. H. Kang, P. G. Rychahou, T. A. Ishola, J. Qiao, B. M. Evers, and D. H. Chung, “MYCN silencing induces differentiation and apoptosis in human neuroblastoma cells,” Biochemical and Biophysical Research Communications, vol. 351, no. 1, pp. 192–197, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Eggert, M. A. Grotzer, N. Ikegaki, X. G. Liu, A. E. Evans, and G. M. Brodeur, “Expression of the neurotrophin receptor TrkA down-regulates expression and function of angiogenic stimulators in SH-SY5Y neuroblastoma cells,” Cancer Research, vol. 62, no. 6, pp. 1802–1808, 2002. View at Google Scholar · View at Scopus
  45. A. Erdreich-Epstein, H. Shimada, S. Groshen et al., “Integrins α(v)β3 and α(v)β5 are expressed by endothelium of high- risk neuroblastoma and their inhibition is associated with increased endogenous ceramide,” Cancer Research, vol. 60, no. 3, pp. 712–721, 2000. View at Google Scholar · View at Scopus
  46. S. Strömblad, J. C. Becker, M. Yebra, P. C. Brooks, and D. A. Cheresh, “Suppression of p53 activity and p21(WAF1/CIP1) expression by vascular cell integrin αvβ3 during angiogenesis,” Journal of Clinical Investigation, vol. 98, no. 2, pp. 426–433, 1996. View at Google Scholar · View at Scopus
  47. J. M. Joseph, N. Gross, N. Lassau et al., “In vivo echographic evidence of tumoral vascularization and microenvironment interactions in metastatic orthotopic human neuroblastoma xenografts,” International Journal of Cancer, vol. 113, no. 6, pp. 881–890, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. D. R. Senger, S. R. Ledbetter, K. P. Claffey, A. Papadopoulos-Sergiou, C. A. Perruzzi, and M. Detmar, “Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the α(v)β3 integrin, osteopontin, and thrombin,” American Journal of Pathology, vol. 149, no. 1, pp. 293–305, 1996. View at Google Scholar · View at Scopus
  49. M. Hirama, F. Takahashi, K. Takahashi et al., “Osteopontin overproduced by tumor cells acts as a potent angiogenic factor contributing to tumor growth,” Cancer Letters, vol. 198, no. 1, pp. 107–117, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Leali, P. Dell'Era, H. Stabile et al., “Osteopontin (Eta-1) and fibroblast growth factor-2 cross-talk in angiogenesis,” Journal of Immunology, vol. 171, no. 2, pp. 1085–1093, 2003. View at Google Scholar · View at Scopus
  51. M. Hecht, J. H. Schulte, A. Eggert, J. Wilting, and L. Schweigerer, “The neurotrophin receptor TrkB cooperates with c-Met in enhancing neuroblastoma invasiveness,” Carcinogenesis, vol. 26, no. 12, pp. 2105–2115, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. W. K. You and D. M. McDonald, “The hepatocyte growth factor/c-met signaling pathway as a therapeutic target to inhibit angiogenesis,” Journal of Biochemistry and Molecular Biology, vol. 41, no. 12, pp. 833–839, 2008. View at Google Scholar · View at Scopus
  53. M. Hecht, M. Papoutsi, H. D. Tran, J. Wilting, and L. Schweigerer, “Hepatocyte growth factor/c-Met signaling promotes the progression of experimental human neuroblastomas,” Cancer Research, vol. 64, no. 17, pp. 6109–6118, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. D. Ribatti and M. Ponzoni, “Antiangiogenic strategies in neuroblastoma,” Cancer Treatment Reviews, vol. 31, no. 1, pp. 27–34, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. J. M. Maris, J. Courtright, P. J. Houghton et al., “Initial testing of the VEGFR inhibitor AZD2171 by the Pediatric Preclinical Testing Program,” Pediatric Blood and Cancer, vol. 50, no. 3, pp. 581–587, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Gomes and P. Rockwell, “p38 MAPK as a negative regulator of VEGF/VEGFR2 signaling pathway in serum deprived human SK-N-SH neuroblastoma cells,” Neuroscience Letters, vol. 431, no. 2, pp. 95–100, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. D. Marimpietri, C. Brignole, B. Nico et al., “Combined therapeutic effects of vinblastine and rapamycin on human neuroblastoma growth, apoptosis, and angiogenesis,” Clinical Cancer Research, vol. 13, no. 13, pp. 3977–3988, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. K. P. Sarker, K. K. Biswas, K. Yamaji et al., “Inhibition of thrombin-induced vascular endothelial growth factor production in human neuroblastoma (NB-1) cells by argatroban,” Pathophysiology of Haemostasis and Thrombosis, vol. 34, no. 1, pp. 41–47, 2005. View at Google Scholar
  59. E. S. Kim, S. Z. Soffer, J. Huang et al., “Distinct response of experimental neuroblastoma to combination antiangiogenic strategies,” Journal of Pediatric Surgery, vol. 37, no. 3, pp. 518–522, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. G. Klement, S. Baruchel, J. Rak et al., “Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity,” Journal of Clinical Investigation, vol. 105, no. 8, pp. R15–R24, 2000. View at Google Scholar · View at Scopus
  61. M. Okuno, S. Kojima, R. Matsushima-Nishiwaki et al., “Retinoids in cancer chemoprevention,” Current Cancer Drug Targets, vol. 4, no. 3, pp. 285–298, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Haque, A. Das, L. M. Hajiaghamohseni, A. Younger, N. L. Banik, and S. K. Ray, “Induction of apoptosis and immune response by all-trans retinoic acid plus interferon-gamma in human malignant glioblastoma T98G and U87MG cells,” Cancer Immunology, Immunotherapy, vol. 56, no. 5, pp. 615–625, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. K. K. Kiningham, Z. A. Cardozo, C. Cook et al., “All-trans-retinoic acid induces manganese superoxide dismutase in human neuroblastoma through NF-κB,” Free Radical Biology and Medicine, vol. 44, no. 8, pp. 1610–1616, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. E. Messi, M. C. Florian, C. Caccia, M. Zanisi, and R. Maggi, “Retinoic acid reduces human neuroblastoma cell migration and invasiveness: effects on DCX, LIS1, neurofilaments-68 and vimentin expression,” BMC Cancer, vol. 8, article no. 30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Holback, L. Adlerz, T. Gatsinzi, K. T. Jacobsen, and K. Iverfeldt, “PI3-K- and PKC-dependent up-regulation of APP processing enzymes by retinoic acid,” Biochemical and Biophysical Research Communications, vol. 365, no. 2, pp. 298–303, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Masiá, S. Alvarez, A. R. De Lera, and D. Barettino, “Rapid, nongenomic actions of retinoic acid on phosphatidylinositol-3-kinase signaling pathway mediated by the retinoic acid receptor,” Molecular Endocrinology, vol. 21, no. 10, pp. 2391–2402, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. M. De los Santos, A. Zambrano, and A. Aranda, “Combined effects of retinoic acid and histone deacetylase inhibitors on human neuroblastoma SH-SY5Y cells,” Molecular Cancer Therapeutics, vol. 6, no. 4, pp. 1425–1432, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Alique, J. F. Herrero, and F. J. Lucio-Cazana, “All-trans retinoic acid induces COX-2 and prostaglandin E2 synthesis in SH-SY5Y human neuroblastoma cells: involvement of retinoic acid receptors and extracellular-regulated kinase 1/2,” Journal of Neuroinflammation, vol. 4, no. 1, pp. 1–9, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Jiang, K. Zhu, J. Grenet, and J. M. Lahti, “Retinoic acid induces caspase-8 transcription via phospho-CREB and increases apoptotic responses to death stimuli in neuroblastoma cells,” Biochimica et Biophysica Acta, vol. 1783, no. 6, pp. 1055–1067, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. J. Cuende, S. Moreno, J. P. Bolaños, and A. Almeida, “Retinoic acid downregulates Rae1 leading to APCCdh1 activation and neuroblastoma SH-SY5Y differentiation,” Oncogene, vol. 27, no. 23, pp. 3339–3344, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. J. S. Wei, C. C. Whiteford, N. Cenacchi, G. S. Chang, and J. Khan, “BBC3 mediates fenretinide-induced cell death in neuroblastoma,” Oncogene, vol. 24, no. 54, pp. 7976–7983, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. Q. D. Campbell Hewson, P. E. Lovat, M. Corazzari, J. B. Catterall, and C. P. F. Redfern, “The NF-κB pathway mediates fenretinide-induced apoptosis in SH-SY5Y neuroblastoma cells,” Apoptosis, vol. 10, no. 3, pp. 493–498, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. I. Casciano, B. Banelli, M. Croce et al., “Caspase-8 gene expression in neuroblastoma,” Annals of the New York Academy of Sciences, vol. 1028, no. 12, pp. 157–167, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. P. E. Lovat, M. Corazzari, B. Goranov, M. Piacentini, and C. P. F. Redfern, “Molecular mechanisms of fenretinide-induced apoptosis of neuroblastoma cells,” Annals of the New York Academy of Sciences, vol. 1028, no. 12, pp. 81–89, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Osone, H. Hosoi, Y. Kuwahara, Y. Matsumoto, T. Iehara, and T. Sugimoto, “Fenretinide induces sustained-activation of JNK/p38 MAPK and apoptosis in a reactive oxygen species-dependent manner in neuroblastoma cells,” International Journal of Cancer, vol. 112, no. 2, pp. 219–224, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Ribatti, G. Alessandri, M. Baronio et al., “Inhibition of neuroblastoma-induced angiogenesis by fenretinide,” International Journal of Cancer, vol. 94, no. 3, pp. 314–321, 2001. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Shusterman, S. A. Grupp, R. Barr, D. Carpentieri, H. Zhao, and J. M. Maris, “The angiogenesis inhibitor TNP-470 effectively inhibits human neuroblastoma xenograft growth, especially in the setting of subclinical disease,” Clinical Cancer Research, vol. 7, no. 4, pp. 977–984, 2001. View at Google Scholar · View at Scopus
  78. C. Yasuda, S. Sakata, S. Kakinoki, Y. Takeyama, H. Ohyanagi, and H. Shiozaki, “In vivo evaluation of microspheres containing the angiogenesis inhibitor, TNP-470, and the metastasis suppression with liver metastatic model implanted neuroblastoma,” Pathophysiology, vol. 17, no. 2, pp. 149–155, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. M. J. Morowitz, R. Barr, Q. Wang et al., “Methionine aminopeptidase 2 inhibition is an effective treatment strategy for neuroblastoma in preclinical models,” Clinical Cancer Research, vol. 11, no. 7, pp. 2680–2685, 2005. View at Publisher · View at Google Scholar · View at Scopus
  80. J. Wang, G. S. Sheppard, P. Lou et al., “Tumor suppression by a rationally designed reversible inhibitor of methionine aminopeptidase-2,” Cancer Research, vol. 63, no. 22, pp. 7861–7869, 2003. View at Google Scholar · View at Scopus
  81. J. Wang, L. A. Tucker, J. Stavropoulos et al., “Correlation of tumor growth suppression and methionine aminopetidase-2 activity blockade using an orally active inhibitor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 6, pp. 1838–1843, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Kuroiwa, H. Ikeda, T. Hongo et al., “Effects of recombinant human endostatin on a human neuroblastoma xenograft,” International Journal of Molecular Medicine, vol. 8, no. 4, pp. 391–396, 2001. View at Google Scholar · View at Scopus
  83. C. Streck, Y. Zhang, J. Zhou et al., “Endostatin-mediated concomitant resistance in neuroblastoma,” Journal of Pediatric Surgery, vol. 39, no. 3, pp. 405–411, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. T. A. Yap and J. S. De Bono, “Targeting the HGF/c-met axis: state of play,” Molecular Cancer Therapeutics, vol. 9, no. 5, pp. 1077–1079, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. H. E. Crosswell, A. Dasgupta, C. S. Alvarado et al., “PHA665752, a small-molecule inhibitor of c-Met, inhibits hepatocyte growth factor-stimulated migration and proliferation of c-Met-positive neuroblastoma cells,” BMC Cancer, vol. 9, no. 11, article 411, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Kuljaca, T. Liu, A. E. L. Tee et al., “Enhancing the anti-angiogenic action of histone deacetylase inhibitors,” Molecular Cancer, vol. 6, no. 10, article 68, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. L. Zhang, K. M. Smith, A. L. Chong et al., “In vivo antitumor and antimetastatic activity of Sunitinib in preclinical Neuroblastoma mouse model,” Neoplasia, vol. 11, no. 5, pp. 426–435, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. P. V. Dickson, J. B. Hamner, T. L. Sims et al., “Bevacizumab-induced transient remodeling of the vasculature in neuroblastoma xenografts results in improved delivery and efficacy of systemically administered chemotherapy,” Clinical Cancer Research, vol. 13, no. 13, pp. 3942–3950, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. Q. Yang, Y. Tian, S. Liu et al., “Thrombospondin-1 peptide ABT-510 combined with valproic acid is an effective antiangiogenesis strategy in neuroblastoma,” Cancer Research, vol. 67, no. 4, pp. 1716–1724, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. G. Pagnan, D. D. Paolo, R. Carosio et al., “The combined therapeutic effects of bortezomib and fenretinide on neuroblastoma cells involve endoplasmic reticulum stress response,” Clinical Cancer Research, vol. 15, no. 4, pp. 1199–1209, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. H. Gong, C. Pöttgen, G. Stüben, W. Havers, M. Stuschke, and L. Schweigerer, “Arginine deiminase and other antiangiogenic agents inhibit unfavorable neuroblastoma growth: potentiation by irradiation,” International Journal of Cancer, vol. 106, no. 5, pp. 723–728, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. J. Cinatl Jr., R. Kotchetkov, R. Blaheta, P. H. Driever, J. U. Vogel, and J. Cinatl, “Induction of differentiation and suppression of malignant phenotype of human neuroblastoma BE(2)-C cells by valproic acid: enhancement by combination with interferon-alpha,” International Journal of Oncology, vol. 20, no. 1, pp. 97–106, 2002. View at Google Scholar · View at Scopus
  93. W. W. Spurbeck, C. Y. C. Ng, E. F. Vanin, and A. M. Davidoff, “Retroviral vector-producer cell-mediated in vivo gene transfer of TIMP-3 restricts angiogenesis and neuroblastoma growth in mice,” Cancer Gene Therapy, vol. 10, no. 3, pp. 161–167, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. A. M. Davidoff, M. A. Leary, C. Y. C. Ng, and E. F. Vanin, “Gene therapy-mediated expression by tumor cells of the angiogenesis inhibitor flk-1 results in inhibition of neuroblastoma growth in vivo,” Journal of Pediatric Surgery, vol. 36, no. 1, pp. 30–36, 2001. View at Publisher · View at Google Scholar · View at Scopus
  95. C. J. Streck, P. V. Dickson, C. Y. C. Ng et al., “Adeno-associated virus vector-mediated systemic delivery of IFN-β combined with low-dose cyclophosphamide affects tumor regression in murine neuroblastoma models,” Clinical Cancer Research, vol. 11, no. 16, pp. 6020–6029, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. Y. Ino, Y. Saeki, H. Fukuhara, and T. Todo, “Triple combination of oncolytic herpes simplex virus-1 vectors armed with interleukin-12, interleukin-18, or soluble B7-1 results in enhanced antitumor efficacy,” Clinical Cancer Research, vol. 12, no. 2, pp. 643–652, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. K. E. Siapati, S. Barker, C. Kinnon et al., “Improved antitumour immunity in murine neuroblastoma using a combination of IL-2 and IL-12,” British Journal of Cancer, vol. 88, no. 10, pp. 1641–1648, 2003. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Croce, R. Meazza, A. M. Orengo et al., “Sequential immunogene therapy with interleukin-12- and interleukin-15- engineered neuroblastoma cells cures metastatic disease in syngeneic mice,” Clinical Cancer Research, vol. 11, no. 2 I, pp. 735–742, 2005. View at Google Scholar · View at Scopus
  99. H. N. Lode, T. Moehler, R. Xiang et al., “Synergy between an antiangiogenic integrin αv antagonist and an antibody-cytokine fusion protein eradicates spontaneous tumor metastases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 4, pp. 1591–1596, 1999. View at Google Scholar · View at Scopus
  100. F. Pastorino, C. Brignole, D. Di Paolo et al., “Targeting liposomal chemotherapy via both tumor cell-specific and tumor vasculature-specific ligands potentiates therapeutic efficacy,” Cancer Research, vol. 66, no. 20, pp. 10073–10082, 2006. View at Publisher · View at Google Scholar · View at Scopus
  101. A. Corti and M. Ponzoni, “Tumor vascular targeting with tumor necrosis factor α and chemotherapeutic drugs,” Annals of the New York Academy of Sciences, vol. 1028, pp. 104–112, 2004. View at Publisher · View at Google Scholar · View at Scopus
  102. F. J. Burrows, J. P. Overholser, and P. E. Thorpe, “Potent antitumor effects of an antitumor endothelial cell immunotoxin in a murine vascular targeting model,” Cell Biophysics, vol. 24-25, no. 1-3, pp. 15–25, 1994. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Roy Choudhury, S. Karmakar, N. L. Banik, and S. K. Ray, “Synergistic efficacy of sorafenib and genistein in growth inhibition by down regulating angiogenic and survival factors and increasing apoptosis through upregulation of p53 and p21 in malignant neuroblastoma cells having N-Myc amplification or non-amplification,” Investigational New Drugs, vol. 28, no. 6, pp. 812–824, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. E. Palmberg, J. I. Johnsen, J. Paulsson et al., “Metronomic scheduling of imatinib abrogates clonogenicity of neuroblastoma cells and enhances their susceptibility to selected chemotherapeutic drugs in vitro and in vivo,” International Journal of Cancer, vol. 124, no. 5, pp. 1227–1234, 2009. View at Google Scholar