Supplemental Blood Circulation System in Hematologic Malignancies

A.A. Vartanyan

N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478

For correspondence: A.A. Vartanyan, DSci, Senior scientific worker, 24 Kashirskoye sh., Moscow, Russian Federation, 115478; Tel: +7(499)324-10-65; e-mail: zhivotov57@mail.ru

For citation: Vartanyan A.A. Supplemental Blood Circulation System in Hematologic Malignancies. Klin. Onkogematol. 2014; 7(4): 491–500 (In Russ.).


ABSTRACT

Neoangiogenesis, i.e. formation of new blood microvessels on the basis of already existing vascular network, is a prerequisite for tumor growth. For years, neoangiogenesis has been considered the only way for delivering oxygen and nutrients to the tumor. However, over the last years, other mechanism of tumor vascularization has been studied. Formation of highly structured vascular channels from tumor cells in the absence of endothelial cells and fibroblasts surrounded by basal membrane, or vasculogenic mimicry (VM) is considered a supplemental blood supply system. VM was found in almost all types of tumors and its occurrence is strongly associated with poor prognosis. This review summarizes basic VM characteristics in solid tumors and hematological malignancies. It also discusses the clinical significance of the above mentioned phenomenon in diagnosing tumors and predicting their course.


Keywords: neoangiogenesis, vasculogenic mimicry, hematological malignancies.

Accepted: September 1, 2014

Read in PDF (RUS)pdficon


REFERENCES 

  1. Persson A., Buschmann I. Vascular growth in health and disease. Front. Mol. Neurosci. 2011; 24: 14–8.
  2. Balaji S., King A., Crombleholme T. et al. The Role of Endothelial Progenitor Cells in Postnatal Vasculogenesis: Implications for Therapeutic Neovascularization and Wound Healing. Adv. Wound Care (New Rochelle). 2013; 2(6): 283–95.
  3. LeBlanc A.J., Krishnan L., Sullivan C.J. et al. Microvascular repair: postangiogenesis vascular dynamics. Microcirculation. 2012; 19(8): 676–95.
  4. Folkman J. New perspectives in clinical oncology from angiogenesis research. Eur. J. Cancer. 1996; 32A(14): 2534–9.
  5. Shibuya M. VEGF-VEGFR Signals in Health and Disease. Biomol. Ther. 2014; 22(1): 1–9.
  6. Vempati P., Popel A.S., MacGabhann S. Extracellular regulation of VEGF: isoforms, proteolysis, and vascular patterning. Cytokine Growth Factor Rev. 2014; 25(1): 1–19.
  7. De Falco S. The discovery of placenta growth factor and its biological activity. Exp. Mol. Med. 2012; 44(1): 1–9.
  8. Lieu C., Heymach J., Overman M. et al. Beyond VEGF: inhibition of the fibroblast growth factor pathway and antiangiogenesis. Clin. Cancer Res. 2011; 17(19): 6130–9.
  9. Hellberg C., Ostman A., Heldin C.H. PDGF and vessel maturation. Recent Results Cancer Res. 2010; 180: 103–14.
  10. Fagiani E., Christofori G. Angiopoietins in angiogenesis. Cancer Lett. 2013; 328(1): 18–26.
  11. Moschetta M., Mishima Y., Sahin I. et al. Role of endothelial progenitor cells in cancer progression. Biochim. Biophys. Acta. 2014; 1846(1): 26–39.
  12. Donnem T., Hu J., Ferguson M. et al. Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment? Cancer Med. 2013; 2(4): 427–36.
  13. Maniotis A.J., Folberg R., Hess A. et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol. 1999; 155(3): 739–52.
  14. Hendrix M.J., Seftor E.A., Hess A.R. et al. Molecular plasticity of human melanoma cells. Oncogene. 2003; 22(20): 3070–5.
  15. Welti J., Loges S., Dimmeler S., Carmeliet P. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J. Clin. Invest. 2013; 123(8): 3190–200.
  16. Cao Z., Bao M., Miele L., Sarkar F.H., Wang Z., Zhou Q. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur. J. Cancer. 2013; 49(18): 3914–23.
  17. Seftor R.E., Hess A.R., Seftor E.A. et al. Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am. J. Pathol. 2012; 181(4): 1115–25.
  18. Fan Y.Z., Sun W. Molecular regulation of vasculogenic mimicry in tumors and potential tumor-target therapy. World J. Gastrointest. Surg. 2010; 2(4): 117–27.
  19. Hess A.R., Seftor E.A., Gruman L.M. et al. VE-cadherin regulates EphA2 in aggressive melanoma cells through a novel signaling pathway: implications for vasculogenic mimicry. Cancer Biol. Ther. 2006; 5(2): 228–33.
  20. Mourad-Zeidan A.A., Melnikova V.O., Wang H. Expression profiling of Galectin-3-depleted melanoma cells reveals its major role in melanoma cell plasticity and vasculogenic mimicry. Am. J. Pathol. 2008; 173(6): 1839–52.
  21. Basu G.D., Pathangey L.B., Tinder T.L. Mechanisms underlying the growth inhibitory effects of the cyclo-oxygenase-2 inhibitor celecoxib in human breast cancer cells. Breast Cancer Res. 2005; 7(4): R422–35.
  22. Vartanian A., Gatsina G., Grigorieva I. et al. The involvement of Notch signaling in melanoma vasculogenic mimicry. Clin. Exp. Med. 2013; 13(3): 201–9.
  23. Vartanian A., Stepanova E., Grigorieva I. et al. Melanoma vasculogenic mimicry capillary-like structure formation depends on integrin and calcium signaling. Microcirculation. 2011; 18(5): 390–9.
  24. Vartanian A., Stepanova E., Grigorieva I. VEGFR1 and PKC control melanoma vasculogenic mimicry in a VEGFR2 kinase-independent manner. Melanoma Res. 2011; 21(2): 91–8.
  25. Lissitzky J.C., Parriaux D., Ristorcelli E. Cyclic AMP signaling as a mediator of vasculogenic mimicry in aggressive human melanoma cells in vitro. Cancer Res. 2009; 69(3): 802–9.
  26. Xi Y., Nakajima G., Hamil T. Association of insulin-like growth factor binding protein-3 expression with melanoma progression. Mol. Cancer Ther. 2006; 5(12): 3078–84.
  27. Hess A.R., Hendrix M.J. Focal adhesion kinase signaling and the aggressive melanoma phenotype. Cell Cycle. 2006; 5(5): 478–80.
  28. Ruf W., Seftor E.A., Petrovan R.J. et al. Differential role of tissue factor pathway inhibitors 1 and 2 in melanoma vasculogenic mimicry. Cancer Res. 2003; 63(17): 5381–9.
  29. Ciurea M.E., Georgescu A.M., Purcaru S.O. Cancer stem cells: biological functions and therapeutically targeting. Int. J. Mol. Sci. 2014; 15(5): 8169–85.
  30. Friedmann-Morvinski D., Verma I.M. Dedifferentiation and reprogramming: origins of cancer stem cells. EMBO Rep. 2014; 15(3): 244–53.
  31. Stewart J.M., Shaw P.A., Geyde C. et al. Phenotypic heterogenity and instability of human ovarian tumor-initiating cells. Proc. Natl. Acad. Sci. USA. 2011; 108(16): 6468–73.
  32. Meier P., Finch A., Evan G. Apoptosis in development. Nature. 2000; 407(6805): 796–801.
  33. Tait S.W., Ichim G., Green D.R. Die another way — non-apoptotic mechanisms of cell death. J. Cell Sci. 2014; 127(Pt. 10): 2135–44.
  34. Vartanian A., Burova O., Stepanova E. et al. The involvement of apoptosis in melanoma vasculogenic mimicry. Mel Res. 2007; 1: 1–8.
  35. Vartanian A., Burova O., Stepanova E. et al. Melanoma vasculogenic mimicry is strongly related to reactice oxygen species level. Mel. Res. 2007; 17(6): 370–9.
  36. Narendhirakannan R.T., Hannah M.A. Oxidative Stress and Skin Cancer: An Overview. Indian J. Clin. Biochem. 2013; 28(2): 110–5.
  37. Holmstrom K.M., Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 2014; 15(6): 411–21.
  38. Brakenhielm E., Cao R., Cao Y. et al. Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound from red wine and grapes. FASEB J. 2001; 15: 1798–800.
  39. Vartanian A., Stepanova E., Grigorieva I. et al. Melanoma vasculogenic mimicry capillary-like structure formation depends on integrin and calcium signaling. Microcirculation. 2011; 18(5): 390–9.
  40. Shirakawa K., Kobayashi H., Heike Y. et al. Hemodynamics in vasculogenic mimicry and angiogenesis of inflammatory breast cancer xenograft. Cancer Res. 2002; 62(2): 560–6.
  41. Folberg R., Rummel V., Ginderdeuren R. et al. The prognostic value of tumor blood vessel morphology in primary uveal melanoma. Ophthalmology. 1993; 100: 1389–98.
  42. Vartanian A., Stepanova E., Baryshnikov A. et al. Prognostic significance of Periodic Acid-Shiff-positive patterns in clear cell renal cell carcinoma. Canad. J. Urol. 2009; 16(4): 4726–31.
  43. Григорьева И.Н., Вишневская Я.В., Абрамов М.Е. и др. Особенности васкуляризации меланомы кожи человека. Забайкальский медицинский вестник. 2011; 2: 12–8.  [Grigor’eva I.N., Vishnevskaya Ya.V., Abramov M.E. et al. Peculiarities of vacularization of human skin melanoma. Zabaikal’skii meditsinskii vestnik. 2011; 2: 12–8. (In Russ.)]
  44. Wang S.Y., Ke Y.Q., Lu G.H. et al. Vasculogenic mimicry is a prognostic factor for postoperative survival in patients with glioblastoma. J. Neurooncol. 2013; 112(3): 339–45.
  45. Lin P., Wang W., Sun B.C. et al. Vasculogenic mimicry is a key prognostic factor for laryngeal squamous cell carcinoma: a new pattern of blood supply. Chin. Med. J. (Engl.) 2012; 125(19): 3445–9.
  46. Liu R., Yang K., Meng C. Vasculogenic mimicry is a marker of poor prognosis in prostate cancer. Cancer Biol. Ther. 2012; 13(7): 527–33.
  47. Wang S.Y., Yu L., Ling G.Q. et al. Vasculogenic mimicry and its clinical significance in medulloblastoma. Cancer Biol. Ther. 2012; 13(5): 341–8.
  48. Liu X.M., Zhang Q.P., Mu Y.G. et al. Clinical significance of vasculogenic mimicry in human gliomas. J. Neurooncol. 2011; 105(2): 173–9.
  49. Liu W.B., Xu G.L., Jia W.D. et al. Prognostic significance and mechanisms of patterned matrix vasculogenic mimicry in hepatocellular carcinoma. Med. Oncol. 2011; 28: S228–38.
  50. Li M., Gu Y., Zhang Z. et al. Vasculogenic mimicry: a new prognostic sign of gastric adenocarcinoma. Pathol. Oncol. Res. 2010; 16(2): 259–66.
  51. Baeten C.I., Hillen F., Pauwels P. et al. Prognostic role of vasculogenic mimicry in colorectal cancer. Dis. Colon Rectum. 2009; 52(12): 2028–35.
  52. Sood A.K., Fletcher M.S., Zahn C.M. et al. The clinical significance of tumor cell-lined vasculature in ovarian carcinoma: implications for anti-vasculogenic therapy. Cancer Biol. Ther. 2002; 1(6): 661–4.
  53. Sun B., Zhang S., Zhao X. et al. Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int. J. Oncol. 2004; 25(6): 1609–14.
  54. Wu S., Yu L., Wang D. et al. Aberrant expression of CD133 in non-small cell lung cancer and its relationship to vasculogenic mimicry. BMC Cancer. 2012; 12: 535–8.
  55. Cameron D., Brown J., Dent R. et al. Adjuvant bevacizumab-containing therapy in triple-negative breast cancer (BEATRICE): primary results of a randomised, phase 3 trial. Lancet Oncol. 2013; 14(10): 933–42.
  56. Corrie P.G., Marshall A., Dunn J.A. et al. Adjuvant bevacizumab in patients with melanoma at high risk of recurrence (AVAST-M): preplanned interim results from a multicentre, open-label, randomised controlled phase 3 study. Lancet Oncol. 2014; 15(6): 620–30.
  57. Dias S., Hattori K., Zhu Z. et al. Autocrine stimulation of VEGFR-2 activates human leukemic cell growth and migration. J. Clin. Invest. 2000; 106: 511–21.
  58. Li W.W., Hutnik M., Gehr G. Antiangiogenesis in haematological malignancies. Br. J. Haematol. 2008; 143(5): 622–31.
  59. Grosicki S., Grosicka A., Holowiecki J. Clinical importance of angiogenesis and angiogenic factors in oncohematology. Wiad. Lek. 2007; 60(1–2): 39–46.
  60. Dimopoulos M.A., Delimpasi S., Katodritou E. et al. Significant improvement in the survival of patients with multiple myeloma presenting with severe renal impairment after the introduction of novel agents. Ann. Oncol. 2014; 25(1): 195–200.
  61. Song G., Li Y., Jiang G. Role of VEGF/VEGFR in the pathogenesis of leukemias and as treatment targets. Oncol. Rep. 2012; 28(6): 1935–44.
  62. Ruan J. Antiangiogenic therapies in non-Hodgkin’s lymphoma. Curr. Cancer Drug Targets. 2011; 11(9): 1030–43.
  63. Gong J.K. Endosteal marrow: a rich source of hematopoietic stem cells. Science. 1978; 199: 1443–45.
  64. Yin T., Li L. The stem cell niches in bone. J. Clin. Invest. 2006; 116(5): 1195–201.
  65. Bradford G.B., Williams B., Rossi R. et al. Quiescence, cycling and turnover in the hematopoietic stem cell compartment. Exp. Hematol. 1997; 25(5): 445–53.
  66. Вартанян А. Основные закономерности ангиогенеза при онкогематологических заболеваниях. Клин. онкогематол. 2013; 6(4): 343–54. [Vartanyan A. Basic principles of angiogenesis in hematological malignancies. Klin. Onkogematol. 2013; 6(4): 343–54. (In Russ.)]
  67. Nico B., Margieri D., Crivellato E. et al. Mast cells contribute to vasculogenic mimicry in multiple myeloma. Stem Cell Dev. 2008; 17(1): 19–22.
  68. Scavelli C., Nico B., Cirulli T. et al. Vasculogenic mimicry by bone marrow macrophages in patients with multiple myeloma. Oncogene. 2008; 27(5): 663–74.
  69. Mirshahi P., Raffi A., Vincent I. et al. Vasculogenic mimicry of acute leukemic bone marrow stromal cells. Leukemia. 2009; 23: 1039–48.
  70. Ding Y.P., Yang X.D., Wu Y. et al. Autophagy promotes the survival and development of tumors by participating in the formation of vasculogenic mimicry. Oncol. Rep. 2014; 31(5): 2321–7.
  71. Mizushima N., Levine B., Cuervo A.M. et al. Autophagy fights disease through cellular selfdigestion. Nature. 2008; 451: 1069–75.
  72. Shimizu S., Yoshida T., Tsujioka M. et al. Autophagic cell death and cancer. Int. J. Mol. Sci. 2014; 15(2): 3145–53.