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BioMed Research International
Volume 2014 (2014), Article ID 986768, 8 pages
http://dx.doi.org/10.1155/2014/986768
Review Article

From Sprouting Angiogenesis to Erythrocytes Generation by Cancer Stem Cells: Evolving Concepts in Tumor Microcirculation

Division of Hematology and Oncology, Faculty of Medicine, American University of Beirut, P.O. Box 11-0236, Riad El Solh, Beirut 1107-2020, Lebanon

Received 9 May 2014; Revised 13 July 2014; Accepted 14 July 2014; Published 4 August 2014

Academic Editor: Shiwu Zhang

Copyright © 2014 Raafat S. Alameddine 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. Z. K. Otrock, R. A. R. Mahfouz, J. A. Makarem, and A. I. Shamseddine, “Understanding the biology of angiogenesis: review of the most important molecular mechanisms,” Blood Cells, Molecules, and Diseases, vol. 39, no. 2, pp. 212–220, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Carmeliet, “Mechanisms of angiogenesis and arteriogenesis,” Nature Medicine, vol. 6, no. 4, pp. 389–395, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. R. S. Alameddine, Z. K. Otrock, A. Awada, and A. Shamseddine, “Crosstalk between HER2 signaling and angiogenesis in breast cancer: molecular basis, clinical applications and challenges,” Current Opinion in Oncology, vol. 25, no. 3, pp. 313–324, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. L. B. Jakeman, M. Armanini, H. S. Phillips, and N. Ferrara, “Developmental expression of binding sites and messenger ribonucleic acid for vascular endothelial growth factor suggests a role for this protein in vasculogenesis and angiogenesis,” Endocrinology, vol. 133, no. 2, pp. 848–859, 1993. View at Publisher · View at Google Scholar · View at Scopus
  5. N. Ferrara, H. Gerber, and J. LeCouter, “The biology of VEGF and its receptors,” Nature Medicine, vol. 9, no. 6, pp. 669–676, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. M. J. Cross, J. Dixelius, T. Matsumoto, and L. Claesson-Welsh, “VEGF-receptor signal transduction,” Trends in Biochemical Sciences, vol. 28, no. 9, pp. 488–494, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Neufeld, S. Tessler, H. Gitay-Goren, T. Cohen, and B. Z. Levi, “Vascular endothelial growth factor and its receptors,” Progress in Growth Factor Research, vol. 5, no. 1, pp. 89–97, 1994. View at Publisher · View at Google Scholar
  8. J. D. Hood, C. J. Meininger, M. Ziche, and H. J. Granger, “VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 274, no. 3, part 2, pp. H1054–H1058, 1998. View at Google Scholar · View at Scopus
  9. K. Miller, M. Wang, J. Gralow et al., “Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer,” The New England Journal of Medicine, vol. 357, no. 26, pp. 2666–2676, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. R. S. Kerbel, “Tumor angiogenesis,” The New England Journal of Medicine, vol. 358, no. 19, pp. 2039–2049, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. J. M. L. Ebos, C. R. Lee, W. Cruz-Munoz, G. A. Bjarnason, J. G. Christensen, and R. S. Kerbel, “Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis,” Cancer Cell, vol. 15, no. 3, pp. 232–239, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Pàez-Ribes, E. Allen, J. Hudock et al., “Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis,” Cancer Cell, vol. 15, no. 3, pp. 220–231, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. D. M. Brizel, G. S. Sibley, L. R. Prosnitz, R. L. Scher, and M. W. Dewhirst, “Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck,” International Journal of Radiation Oncology Biology Physics, vol. 38, no. 2, pp. 285–289, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Höckel, K. Schlenger, B. Aral, M. Mitze, U. Schäffer, and P. Vaupel, “Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix,” Cancer Research, vol. 56, no. 19, pp. 4509–4515, 1996. View at Google Scholar · View at Scopus
  15. S. Walenta, A. Salameh, H. Lyng et al., “Correlation of high lactate levels in head and neck tumors with incidence of metastasis,” The American Journal of Pathology, vol. 150, no. 2, pp. 409–415, 1997. View at Google Scholar · View at Scopus
  16. G. Pitson, A. Fyles, M. Milosevic, J. Wylie, M. Pintilie, and R. Hill, “Tumor size and oxygenation are independent predictors of nodal diseases in patients with cervix cancer,” International Journal of Radiation Oncology Biology Physics, vol. 51, no. 3, pp. 699–703, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Holash, P. C. Maisonpierre, D. Compton et al., “Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF,” Science, vol. 284, no. 5422, pp. 1994–1998, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Donnem, J. Hu, M. Ferguson et al., “Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment?” Cancer Medicine, vol. 2, no. 4, pp. 427–436, 2013. View at Google Scholar
  19. P. B. Vermeulen, C. Colpaert, R. Salgado et al., “Liver metastases from colorectal adenocarcinomas grow in three patterns with different angiogenesis and desmoplasia,” Journal of Pathology, vol. 195, no. 3, pp. 336–342, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. W. P. J. Leenders, B. Küsters, K. Verrijp et al., “Antiangiogenic therapy of cerebral melanoma metastases results in sustained tumor progression via vessel co-option,” Clinical Cancer Research, vol. 10, no. 18 I, pp. 6222–6230, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. A. D. Smith, S. N. Shah, B. I. Rini, M. L. Lieber, and E. M. Remer, “Morphology, Attenuation, Size, and Structure (MASS) criteria: assessing response and predicting clinical outcome in metastatic renal cell carcinoma on antiangiogenic targeted therapy,” American Journal of Roentgenology, vol. 194, no. 6, pp. 1470–1478, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. J. C. Welti, T. Powles, S. Foo et al., “Contrasting effects of sunitinib within in vivo models of metastasis,” Angiogenesis, vol. 15, no. 4, pp. 623–641, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Hu, F. Bianchi, M. Ferguson et al., “Gene expression signature for angiogenic and nonangiogenic non-small-cell lung cancer,” Oncogene, vol. 24, no. 7, pp. 1212–1219, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. F. Stessels, G. van den Eynden, I. van der Auwera et al., “Breast adenocarcinoma liver metastases, in contrast to colorectal cancer liver metastases, display a non-angiogenic growth pattern that preserves the stroma and lacks hypoxia,” British Journal of Cancer, vol. 90, no. 7, pp. 1429–1436, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. J. H. Caduff, L. C. Fischer, and P. H. Burri, “Scanning electron microscope study of the developing microvasculature in the postnatal rat lung,” Anatomical Record, vol. 216, no. 2, pp. 154–164, 1986. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Patan, L. L. Munn, and R. K. Jain, “Intussusceptive microvascular growth in a human colon adenocarcinoma xenograft: a novel mechanism of tumor angiogenesis,” Microvascular Research, vol. 51, no. 2, pp. 260–272, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Hlushchuk, O. Riesterer, O. Baum et al., “Tumor recovery by angiogenic switch from sprouting to intussusceptive angiogenesis after treatment with PTK787/ZK222584 or ionizing radiation,” American Journal of Pathology, vol. 173, no. 4, pp. 1173–1185, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Djonov, O. Baum, and P. H. Burri, “Vascular remodeling by intussusceptive angiogenesis,” Cell and Tissue Research, vol. 314, no. 1, pp. 107–117, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. V. Djonov, M. Schmid, S. A. Tschanz, and P. H. Burri, “Intussusceptive angiogenesis: its role in embryonic vascular network formation,” Circulation Research, vol. 86, no. 3, pp. 286–292, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Collen, R. Hanemaaijer, F. Lupu et al., “Membrane-type matrix metalloproteinase-mediated angiogenesis in a fibrin-collagen matrix,” Blood, vol. 101, no. 5, pp. 1810–1817, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. G. W. Prager, J. M. Breuss, S. Steurer, J. Mihaly, and B. R. Binder, “Vascular endothelial growth factor (VEGF) induces rapid prourokinase (pro-uPA) activation on the surface of endothelial cells,” Blood, vol. 103, no. 3, pp. 955–962, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. M. C. Brahimi-Horn, J. Chiche, and J. Pouysségur, “Hypoxia and cancer,” Journal of Molecular Medicine, vol. 85, no. 12, pp. 1301–1307, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. B. Bao, A. S. Azmi, S. Ali et al., “The biological kinship of hypoxia with CSC and EMT and their relationship with deregulated expression of miRNAs and tumor aggressiveness,” Biochimica et Biophysica Acta, vol. 1826, no. 2, pp. 272–296, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. M. K. Asiedu, J. N. Ingle, M. D. Behrens, D. C. Radisky, and K. L. Knutson, “TGFβ/TNFα-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype,” Cancer Research, vol. 71, no. 13, pp. 4707–4719, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. E. D. Hay, “An overview of epithelio-mesenchymal transformation,” Acta Anatomica, vol. 154, no. 1, pp. 8–20, 1995. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Hugo, M. L. Ackland, T. Blick et al., “Epithelial—mesenchymal and mesenchymal—epithelial transitions in carcinoma progression,” Journal of Cellular Physiology, vol. 213, no. 2, pp. 374–383, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. A. M. Shannon, D. J. Bouchier-Hayes, C. M. Condron, and D. Toomey, “Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies,” Cancer Treatment Reviews, vol. 29, no. 4, pp. 297–307, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Schreck, K. Albermann, and P. A. Baeuerle, “Nuclear factor κβ: an oxidative stress-responsive transcription factor of eukaryotic cells (a review),” Free Radical Research Communications, vol. 17, no. 4, pp. 221–237, 1992. View at Publisher · View at Google Scholar · View at Scopus
  39. A. C. Koong, E. Y. Chen, and A. J. Giaccia, “Hypoxia causes the activation of nuclear factor κB through the phosphorylation of IκBα on tyrosine residues,” Cancer Research, vol. 54, no. 6, pp. 1425–1430, 1994. View at Google Scholar · View at Scopus
  40. M. A. Huber, N. Azoitei, B. Baumann et al., “NF-κB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression,” Journal of Clinical Investigation, vol. 114, no. 4, pp. 569–581, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. Z. Cheng, B. Sun, S. Wang et al., “Nuclear factor-κB-dependent epithelial to mesenchymal transition induced by HIF-1α activation in pancreatic cancer cells under hypoxic conditions,” PLoS ONE, vol. 6, no. 8, Article ID e23752, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. W. Yan, Y. Fu, D. Tian et al., “PI3 kinase/Akt signaling mediates epithelial-mesenchymal transition in hypoxic hepatocellular carcinoma cells,” Biochemical and Biophysical Research Communications, vol. 382, no. 3, pp. 631–636, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. G. Lin, R. Gai, Z. Chen et al., “The dual PI3K/mTOR inhibitor NVP-BEZ235 prevents epithelial-mesenchymal transition induced by hypoxia and TGF-beta1,” European Journal of Pharmacology, vol. 729, pp. 45–53, 2014. View at Publisher · View at Google Scholar
  44. L. Miele, “Notch signaling,” Clinical Cancer Research, vol. 12, no. 4, pp. 1074–1079, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Ishida, H. Hijioka, K. Kume, A. Miyawaki, and N. Nakamura, “Notch signaling induces EMT in OSCC cell lines in a hypoxic environment,” Oncology Letters, vol. 6, no. 5, pp. 1201–1206, 2013. View at Google Scholar
  46. J. Chen, N. Imanaka, and J. D. Griffin, “Hypoxia potentiates Notch signaling in breast cancer leading to decreased E-cadherin expression and increased cell migration and invasion,” British Journal of Cancer, vol. 102, no. 2, pp. 351–360, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. R. Fodde and T. Brabletz, “Wnt/β-catenin signaling in cancer stemness and malignant behavior,” Current Opinion in Cell Biology, vol. 19, no. 2, pp. 150–158, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Nusse and H. E. Varmus, “Wnt genes,” Cell, vol. 69, no. 7, pp. 1073–1087, 1992. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Y. Logan and R. Nusse, “The Wnt signaling pathway in development and disease,” Annual Review of Cell and Developmental Biology, vol. 20, pp. 781–810, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. G. Jiang, Y. Luo, D. L. He et al., “Role of Wnt/β-catenin signaling pathway in epithelial-mesenchymal transition of human prostate cancer induced by hypoxia-inducible factor-1α,” International Journal of Urology, vol. 14, no. 11, pp. 1034–1039, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. S. K. To, W. J. Zeng, J. Z. Zeng, and A. S. Wong, “Hypoxia triggers a Nur77-beta-catenin feed-forward loop to promote the invasive growth of colon cancer cells,” The British Journal of Cancer, vol. 110, no. 4, pp. 935–945, 2014. View at Google Scholar
  52. L. Liu, X. Zhu, W. Wang et al., “Activation of β-catenin by hypoxia in hepatocellular carcinoma contributes to enhanced metastatic potential and poor prognosis,” Clinical Cancer Research, vol. 16, no. 10, pp. 2740–2750, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. M. P. Di Magliano and M. Hebrok, “Hedgehog signalling in cancer formation and maintenance,” Nature Reviews Cancer, vol. 3, no. 12, pp. 903–911, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. A. Yoo, M. H. Kang, H. J. Lee et al., “Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer,” Cancer Research, vol. 71, no. 22, pp. 7061–7070, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Lei, J. Ma, Q. Ma et al., “Hedgehog signaling regulates hypoxia induced epithelial to mesenchymal transition and invasion in pancreatic cancer cells via a ligand-independent manner,” Molecular Cancer, vol. 12, no. 1, article 66, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Onishi, M. Kai, S. Odate et al., “Hypoxia activates the hedgehog signaling pathway in a ligand-independent manner by upregulation of Smo transcription in pancreatic cancer,” Cancer Science, vol. 102, no. 6, pp. 1144–1150, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. A. J. Maniotis, R. Folberg, A. Hess et al., “Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry,” The American Journal of Pathology, vol. 155, no. 3, pp. 739–752, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. M. J. C. Hendrix, E. A. Seftor, A. R. Hess, and R. E. B. Seftor, “Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma,” Nature Reviews Cancer, vol. 3, no. 6, pp. 411–421, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Francescone, S. Scully, B. Bentley et al., “Glioblastoma-derived tumor cells induce vasculogenic mimicry through Flk-1 protein activation,” The Journal of Biological Chemistry, vol. 287, no. 29, pp. 24821–24831, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Scully, R. Francescone, M. Faibish et al., “Transdifferentiation of glioblastoma stem-like cells into mural cells drives vasculogenic mimicry in glioblastomas,” Journal of Neuroscience, vol. 32, no. 37, pp. 12950–12960, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. R. E. B. Seftor, E. A. Seftor, N. Koshikawa et al., “Cooperative interactions of laminin 5 γ2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma,” Cancer Research, vol. 61, no. 17, pp. 6322–6327, 2001. View at Google Scholar · View at Scopus
  62. N. Zhao, B. C. Sun, T. Sun et al., “Hypoxia-induced vasculogenic mimicry formation via VE-cadherin regulation by Bcl-2,” Medical Oncology, vol. 29, no. 5, pp. 3599–3607, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. A. R. Hess, E. A. Seftor, L. M. Gruman, M. S. Kinch, R. E. B. Seftor, and M. J. C. Hendrix, “VE-cadherin regulates EphA2 in aggressive melanoma cells through a novel signaling pathway: implications for vasculogenic mimicry,” Cancer Biology and Therapy, vol. 5, no. 2, pp. 228–233, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. D. W. J. van der Schaft, F. Hillen, P. Pauwels et al., “Tumor cell plasticity in Ewing sarcoma, an alternative circulatory system stimulated by hypoxia,” Cancer Research, vol. 65, no. 24, pp. 11520–11528, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. N. Sharma, R. E. B. Seftor, E. A. Seftor et al., “Prostatic tumor cell plasticity involves cooperative interactions of distinct phenotypic subpopulations: role in vasculogenic mimicry,” Prostate, vol. 50, no. 3, pp. 189–201, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. S. Chen and Z. P. Chen, “Vasculogenic mimicry: a novel target for glioma therapy,” Chinese Journal of Cancer, vol. 33, no. 2, pp. 74–79, 2014. View at Google Scholar
  67. C. I. M. Baeten, F. Hillen, P. Pauwels, A. P. de Bruine, and C. G. M. I. Baeten, “Prognostic role of vasculogenic mimicry in colorectal cancer,” Diseases of the Colon and Rectum, vol. 52, no. 12, pp. 2028–2035, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Wolk, “Considerations on the possible origins of fetal hemoglobin cells produced in developing tumors,” Stem Cells and Development, vol. 23, no. 8, pp. 791–795, 2014. View at Publisher · View at Google Scholar
  69. E. Szabo, S. Rampalli, R. M. Risueño et al., “Direct conversion of human fibroblasts to multilineage blood progenitors,” Nature, vol. 468, no. 7323, pp. 521–526, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Zhang, I. Mercado-Uribe, and J. Liu, “Generation of erythroid cells from fibroblasts and cancer cells in vitro and in vivo,” Cancer Letters, vol. 333, no. 2, pp. 205–212, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Zhang, I. Mercado-Uribe, and J. Liu, “Tumor stroma and differentiated cancer cells can be originated directly from polyploid giant cancer cells induced by paclitaxel,” International Journal of Cancer, vol. 134, no. 3, pp. 508–518, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. T. Yang, K. Rycaj, Z. Liu, and D. G. Tang, “Cancer stem cells: constantly evolving and functionally heterogeneous therapeutic targets,” Cancer Research, vol. 74, no. 11, pp. 2922–2927, 2014. View at Publisher · View at Google Scholar
  73. M. Castedo, J. Perfettini, T. Roumier, K. Andreau, R. Medema, and G. Kroemer, “Cell death by mitotic catastrophe: a molecular definition,” Oncogene, vol. 23, no. 16, pp. 2825–2837, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. D. Zhang, Y. Wang, and S. Zhang, “Asymmetric cell division in polyploid giant cancer cells and low eukaryotic cells,” BioMed Research International, vol. 2014, Article ID 432652, 8 pages, 2014. View at Publisher · View at Google Scholar
  75. J. Erenpreisa and M. S. Cragg, “Three steps to the immortality of cancer cells: senescence, polyploidy and self-renewal,” Cancer Cell International, vol. 13, no. 1, article 92, 2013. View at Google Scholar
  76. Y. Qu, L. Zhang, Z. Rong, T. He, and S. Zhang, “Number of glioma polyploid giant cancer cells (PGCCs) associated with vasculogenic mimicry formation and tumor grade in human glioma,” Journal of Experimental & Clinical Cancer Research, vol. 32, no. 1, p. 75, 2013. View at Publisher · View at Google Scholar
  77. T. M. Illidge, M. S. Cragg, B. Fringes, P. Olive, and J. A. Erenpreisa, “Polyploid giant cells provide a survival mechanism for p53 mutant cells after DNA damage,” Cell Biology International, vol. 24, no. 9, pp. 621–633, 2000. View at Publisher · View at Google Scholar · View at Scopus
  78. S. Zhang, I. Mercado-Uribe, Z. Xing, B. Sun, J. Kuang, and J. Liu, “Generation of cancer stem-like cells through the formation of polyploid giant cancer cells,” Oncogene, vol. 33, no. 1, pp. 116–128, 2014. View at Publisher · View at Google Scholar · View at Scopus