Advanced research on vasculogenic mimicry in cancer

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 2, 2015, Pages 315-326

  Qiao, Lili ^a   Liang, Ning ^b   Zhang, Jiandong ^b   Xie, Jian ^c   Liu, Fengjun ^b   Xu, Deguo ^b   Yu, Xinshuang ^b   Tian, Yuan ^b  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b THE FIRST AFFILIATED HOSPITAL OF SHANDONG FIRST MEDICAL UNIVERSITY   (China)

^c Zhangqiu People's Hospital   (China)

Author keywords

Cancer stem cell; High aggressive tumour; Molecular regulation; Prognosis; Tumour target therapy; Vasculogenic mimicry

Indexed keywords

ANIMAL; CANCER STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION;

EID: 84921655519     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12496     Document Type: Article

References (153)

1. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011; 473: 298-307.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144: 646-74.
3. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000; 100: 57-70.
4. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell. 2011; 146: 873-87.
5. Maniotis AJ, 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: 739-52.
6. Folberg R, Hendrix MJ, Maniotis AJ. Vasculogenic mimicry and tumor angiogenesis. Am J Pathol. 2000; 156: 361-81.
7. Bittner M, Meltzer P, Chen Y, et al. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature. 2000; 406: 536-40.
8. Paulis YW, Soetekouw PM, Verheul HM, et al. Signalling pathways in vasculogenic mimicry. Biochim Biophys Acta. 2010; 1806: 18-28.
9. Cao Z, Yu D, Fu S, et al. Lycorine hydrochloride selectively inhibits human ovarian cancer cell proliferation and tumor neovascularization with very low toxicity. Toxicol Lett. 2013; 218: 174-85.
10. Hess AR, Margaryan NV, Seftor EA, et al. Deciphering the signaling events that promote melanoma tumor cell vasculogenic mimicry and their link to embryonic vasculogenesis: role of the Eph receptors. Dev Dyn. 2007; 236: 3283-96.
11. Mei J, Jia YW, Cai XS. Vascular channel formation by osteosarcoma cells in vitro: vasculogenic mimicry. Chin-German J Clin Oncol. 2003; 2: 237-9.
12. van der Schaft DW, Seftor RE, Seftor EA, et al. Effects of angiogenesis inhibitors on vascular network formation by human endothelial and melanoma cells. J Natl Cancer Inst. 2004; 96: 1473-7.
13. Sun T, Zhao N, Zhao XL, et al. Expression and functional significance of Twist1 in hepatocellular carcinoma: its role in vasculogenic mimicry. Hepatology. 2010; 51: 545-56.
14. Sharma N, Seftor RE, Seftor EA, et al. Prostatic tumor cell plasticity involves cooperative interactions of distinct phenotypic subpopulations: role in vasculogenic mimicry. Prostate. 2002; 50: 189-201.
15. Yue WY, Chen ZP. Does vasculogenic mimicry exist in astrocytoma? J Histochem Cytochem. 2005; 53: 997-1002.
16. EI Hallani S, Boisselier B, Peglion F, et al. A new alternative mechanism in glioblastoma vascularization: tubular vasculogenic mimicry. Brain. 2010; 133: 973-82.
17. Sun W, Shen ZY, Zhang H, et al. Overexpression of HIF-1α in primary gallbladder carcinoma and its relation to vasculogenic mimicry and unfavourable prognosis. Oncol Rep. 2012; 27: 1990-2002.
18. Fujimoto A, Onodera H, Mori A, et al. Tumour plasticity and extravascular circulation in ECV304 human bladder carcinoma cells. Anticancer Res. 2006; 26: 59-69.
19. Sood AK, Seftor EA, Fletcher MS, et al. Molecular determinants of ovarian cancer plasticity. Am J Pathol. 2001; 158: 1279-88.
20. Du J, Sun B, Zhao X, et al. Hypoxia promotes vasculogenic mimicry formation by inducing epithelial- mesenchymal transition in ovarian carcinoma. Gynecol Oncol. 2014; 133: 575-83.
21. Su M, Wei W, Xu X, et al. Role of hCG in vasculogenic mimicry in OVCAR-3 ovarian cancer cell line. Int J Gynecol Cancer. 2011; 21: 1366-74.
22. Wu S, Yu L, Cheng Z, et al. Expression of maspin in non-small cell lung cancer and its relationship to vasculogenic mimicry. J Huazhong Univ Sci Technolog Med Sci. 2012; 32: 346-52.
23. Liu WB, Xu GL, Jia WD, et al. Prognostic significance and mechanisms of patterned matrix vasculogenic mimicry in hepatocellular carcinoma. Med Oncol. 2011; 28: S228-38.
24. Shirakawa K, Kobayashi H, Heike Y, et al. Hemodynamics in vasculogenic mimicry and angiogenesis of inflammatory breast cancer xenograft. Cancer Res. 2002; 62: 560-6.
25. Cai XS, Jia YW, Mei J, et al. Tumor blood vessels formation in osteosarcoma: vasculogenesis mimicry. Chin Med J (Engl). 2004; 117: 94-8.
26. Jiang J, Liu W, Guo X, et al. IRX1 influences peritoneal spreading and metastasis via inhibiting BDKRB2-dependent neovascularization on gastric cancer. Oncogene. 2011; 30: 4498-508.
27. Li M, Gu Y, Zhang Z, et al. Vasculogenic mimicry: a new prognostic sign of gastric adenocarcinoma. Pathol Oncol Res. 2010; 16: 259-66.
28. Kirschmann DA, Seftor EA, Hardy KM, et al. Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin Cancer Res. 2012; 18: 2726-32.
29. Hendrix MJ, Seftor EA, Meltzer PS, et al. Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry. Proc Natl Acad Sci USA. 2001; 98: 8018-23.
30. Hess AR, Seftor EA, Gruman LM, et al. VE-cadherin regulates EphA2 in aggressive melanoma cells through a novel signaling pathway: implications for vasculogenic mimicry. Cancer Biol Ther. 2006; 5: 228-33.
31. Hess AR, Seftor EA, Gardner LM, et al. Molecular regulation of tumor cell vasculogenic mimicry by tyrosine phosphorylation: role of epithelial cell kinase (Eck/EphA2). Cancer Res. 2001; 61: 3250-5.
32. Margaryan NV, Strizzi L, Abbott DE, et al. EphA2 as a promoter of melanoma tumorigenicity. Cancer Biol Ther. 2009; 8: 279-88.
33. Seftor RE, Seftor EA, Koshikawa N, et al. Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res. 2001; 61: 6322-7.
34. Seftor RE, Seftor EA, Kirschmann DA, et al. Targeting the tumor microenvironment with chemically modified tetracyclines: inhibition of laminin 5 gamma2 chain promigratory fragments and vasculogenic mimicry. Mol Cancer Ther. 2002; 1: 1173-9.
35. Hess AR, Seftor EA, Seftor RE, et al. Phosphoinositide 3-kinase regulates membrane Type 1-matrix metalloproteinase (MMP) and MMP-2 activity during melanoma cell vasculogenic mimicry. Cancer Res. 2003; 63: 4757-62.
36. Sood AK, Fletcher MS, Coffin JE, et al. Functional role of matrix metalloproteinases in ovarian tumor cell plasticity. Am J Obstet Gynecol. 2004; 190: 899-909.
37. Su M, Feng YJ, Yao LQ, et al. Plasticity of ovarian cancer cell SKOV3ip and vasculogenic mimicry in vivo. Int J Gynecol Cancer. 2008; 18: 476-86.
38. Hess AR, Hendrix MJ. Focal adhesion kinase signaling and the aggressive melanoma henotype. Cell Cycle. 2006; 5: 478-80.
39. Hess AR, Postovit LM, Margaryan NV, et al. Focal adhesion kinase promotes the aggressive melanoma phenotype. Cancer Res. 2005; 65: 9851-60.
40. Wolf JE Jr, Hubler WR Jr. Tumor angiogenic factor and human skin tumors. Arch Dermatol. 1975; 111: 321-7.
41. Warren BA, Shubik P. The growth of the blood supply to melanoma transplants in the hamster cheek pouch. Lab Invest. 1966; 15: 464-78.
42. Schumacker PT, Samsel RW. Analysis of oxygen delivery and uptake relationships in the Krogh tissue model. J Appl Physiol. 1989; 67: 1234-44.
43. 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: 1609-14.
44. Folberg R, Rummelt V, Parys-Van Ginderdeuren R, et al. The prognostic value of tumor blood vessel morphology in primary uveal melanoma. Ophthalmology. 1993; 100: 1389-98.
45. Clarijs R, Otte-Holler I, Ruiter DJ, et al. Presence of a fluid-conducting meshwork in xenografted cutaneous and primary human uveal melanoma. Invest Ophthalmol Vis Sci. 2002; 43: 912-8.
46. Kobayashi H, Shirakawa K, Kawamoto S, et al. Rapid accumulation and internalization of radiolabeled herceptin in an inflammatory breast cancer xenograft with vasculogenic mimicry predicted by the contrast-enhanced dynamic MRI with the macromolecular contrast agent G6-(1B4MGd)(256). Cancer Res. 2002; 62: 860-6.
47. Maniotis AJ, Chen X, Garcia C, et al. Control of melanoma morphogenesis, endothelial survival, and perfusion by extracellular matrix. Lab Invest. 2002; 82: 1031-43.
48. Link W, Rosado A, Fominaya J, et al. Membrane localization of all class I PI 3-kinase isoforms suppresses c-Myc-induced apoptosis in Rat1 fibroblasts via Akt. J Cell Biochem. 2005; 95: 979-89.
49. Del Peso L, Gonzalez-Garcia M, Page C, et al. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science. 1997; 278: 687-9.
50. Datta SR, Dudek H, Tao X, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997; 91: 231-41.
51. Donepudi M, Grutter MG. Structure and zymogen activation of caspases. Biophys Chem. 2002; 101-102: 145-53.
52. Cardone MH, Roy N, Stennicke HR, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science. 1998; 282: 1318-21.
53. Burgering BM, Medema RH. Decisions on life and death: FOXO Forkhead transcription factors are in command when Akt/PKB is off duty. J Leukoc Biol. 2003; 73: 689-701.
54. Barkett M, Gilmore TD. Control of apoptosis by Rel/NF- κB transcription factors. Oncogene. 1999; 18: 6910-24.
55. Lauder A, Castellanos A, Weston K. c-Myb transcription is activated by protein kinase B (PKB) following interleukin 2 stimulation of T cells and is required for PKB-mediated protection from apoptosis. Mol Cell Biol. 2001; 21: 5797-805.
56. Mayo LD, Donner DB. A phosphatidylinositol 3- kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA. 2001; 98: 11598-603.
57. Gottlieb TM, Leal JF, Seger R, et al. Cross-talk between Akt, p53 and Mdm2: possible implications for the regulation of apoptosis. Oncogene. 2002; 21: 1299-303.
58. Fan YZ, Sun W. Molecular regulation of vasculogenic mimicry in tumors and potential tumor-target therapy. World J Gastrointest Surg. 2010; 2: 117-27.
59. Brantley DM, Cheng N, Thompson EJ, et al. Soluble EphA receptors inhibit tumor angiogenesis and progression in vivo. Oncogene. 2002; 21: 7011-26.
60. Cheng N, Brantley DM, Liu H, et al. Blockade of EphA receptor tyrosine kinase activation inhibits vascular endothelial cell growth factor-induced angiogenesis. Mol Cancer Res. 2002; 1: 2-11.
61. Mackman N. Role of tissue factor in hemostasis, thrombosis, and vascular development. Arterioscler Thromb Vasc Biol. 2004; 24: 1015-22.
62. Gale AJ, Gordon SG. Update on tumor cell procoagulant factors. Acta Haematol. 2001; 106: 25-32.
63. Abdulkadir SA, Carvalhal GF, Kaleem Z, et al. Tissue factor expression and angiogenesis in human prostate carcinoma. Hum Pathol. 2000; 31: 443-7.
64. Ueda C, Hirohata Y, Kihara Y, et al. Pancreatic cancer complicated by disseminated intravascular coagulation associated with production of tissue factor. J Gastroenterol. 2001; 36: 848-50.
65. Carmeliet P, Mackman N, Moons L, et al. Role of tissue factor in embryonic blood vessel development. Nature. 1996; 383: 73-5.
66. Contrino J, Hair G, Kreutzer DL, et al. In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med. 1996; 2: 209-15.
67. Ruf W, Seftor EA, Petrovan RJ, et al. Differential role of tissue factor pathway inhibitors 1 and 2 (TFPI-1 and 2) in melanoma vasculogenic mimicry. Cancer Res. 2003; 63: 5381-9.
68. Vartanian AA, Burova OS, Stepanova EV, et al. The involvement of apoptosis in melanoma vasculogenic mimicry. Melanoma Res. 2007; 17: 1-8.
69. Wang JY, Sun T, Zhao XL, et al. Functional significance of VEGF-A in human ovarian carcinoma: role in vasculogenic mimicry. Cancer Biol Ther. 2008; 7: 758-66.
70. Mei J, Gao Y, Zhang L, et al. VEGF-siRNA silencing induces apoptosis, inhibits proliferation and suppresses vasculogenic mimicry in osteosarcoma in vitro. Exp Oncol. 2008; 30: 29-34.
71. Brantley-Sieders DM, Fang WB, Hwang Y, et al. Ephrin-A1 facilitates mammary tumor metastasis through an angiogenesis-dependent mechanism mediated by EphA receptor and vascular endothelial growth factor in mice. Cancer Res. 2006; 66: 10315-24.
72. Tallquist MD, Soriano P, Kinghoffer RA. Growth factor signaling pathways in vascula development. Oncogene. 1999; 18: 7917-32.
73. Sharma PS, Sharma R, Tyagi T. VEGF/VEGFR pathway inhibitors as anti-angiogenic agents: present and future. Curr Cancer Drug Targets. 2011; 11: 624-53.
74. Takenada K. Angiogenic signaling aberrantly induced by tumor hypoxia. Front Biosci. 2011; 16: 31-48.
75. Semenza GL. Expression of hypoxia-(2000) inducible factor 1: mechanisms and consequences. Biochem Pharmacol. 2000; 59: 47-53.
76. Jones MK, Szabó IL, Kawanaka H, et al. von Hippel Lindau tumor suppressor and HIF-1alpha: new targets of NSAIDs inhibition of hypoxia-induced angiogenesis. FASEB J. 2002; 16: 264-6.
77. Sun B, Zhang D, Zhang S, et al. Hypoxia influences vasculogenic mimicry channel formation and tumor invasion-related protein expression in melanoma. Cancer Lett. 2007; 249: 188-97.
78. Lau KS, Dennis JW. N-Glycans in cancer progression. Glycobiology. 2008; 18: 750-60.
79. Ochieng J, Furtak V, Lukyanov P. Extracellular functions of galectin-3. Glycoconj J. 2004; 19: 527-35.
80. Cassarino DS, Derienzo DP, Barr RJ. Cutaneous squamous cell carcinoma: a comprehensive clinicopathologic classification. Part one. J Cutan Pathol. 2006; 33: 191-206.
81. Krześlak A, Lipińska A. Galectin-3 as a multifunctional protein. Cell Mol Biol Lett. 2004; 9: 305-28.
82. Yoshii T, Fukumori T, Honjo Y, et al. Galectin-3 phosphorylation is required for its anti-apoptotic function and cell cycle arrest. J Biol Chem. 2002; 277: 6852-7.
83. Mourad-Zeidan AA, Melnikova VO, Wang H, et al. Expression profiling of Galectin-3-depleted melanoma cells reveals its major role in melanoma cell plasticity and vasculogenic mimicry. Am J Pathol. 2008; 173: 1839-52.
84. Lissitzky JC, Parriaux D, Ristorcelli E, et al. Cyclic AMP signaling as a mediator of vasculogenic mimicry in aggressive human melanoma cells in vitro. Cancer Res. 2009; 69: 802-9.
85. Postovit LM, Margaryan NV, Seftor EA, et al. Role of nodal signaling and the microenvironment underlying melanoma plasticity. Pigment Cell Melanoma Res. 2008; 21: 348-57.
86. Topczewska JM, Postovit LM, Margaryan NV, et al. Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nat Med. 2006; 12: 925-32.
87. Basu GD, Liang WS, Stephan DA, et al. A novel role for cyclooxygenase-2 in regulating vascular channel formation by human breast cancer cells. Breast Cancer Res. 2006; 8: R69.
88. Luo H, Chen Z, Jin H, et al. Cyclooxygenase-2 up-regulates vascular endothelial growth factor via a protein kinase C pathway in non-small cell lung cancer. J Exp Clin Canc Res. 2011; 30: 6-10.
89. Andres-Barquin PJ, Hernandez MC, Israel MA. Id genes in nervous system development. Histol Histopathol. 2000; 15: 603-18.
90. Benezra R. Role of Id proteins in embryonic and tumor angiogenesis. Trends Cardiovasc Med. 2001; 11: 237-41.
91. Ruzinova MB, Benezra R. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 2003; 13: 410-8.
92. Su F, Li B, Wang J, et al. Molecular regulation of vasculogenic mimicry in human uveal melanoma cells: role of helix-loop-helix Id2 (inhibitor of DNA binding 2). Graefes Arch Clin Exp Ophthalmol. 2009; 247: 411-9.
93. Petty AP, Garman KL, Winn VD, et al. Overexpression of carcinoma and embryonic cytotrophoblast cell-specific Mig-7 induces invasion and vessel-like structure formation. Am J Pathol. 2007; 170: 1763-80.
94. Crawford ED, Seaman JE, Barber AE 2nd, et al. Conservation of caspase substrates across metazoans suggests hierarchical importance of signaling pathways over specific targets and cleavage site motifs in apoptosis. Cell Death Differ. 2012; 19: 2040-8.
95. Hyman BT, Yuan J. Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat Rev Neurosci. 2012; 13: 395-406.
96. Chun HJ, Zheng L, Ahmad M, et al. Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature. 2002; 419: 395-9.
97. Su H, Bidere N, Zheng L, et al. Requirement for caspase-8 in NF-kappaB activation by antigen receptor. Science. 2005; 307: 1465-8.
98. Van Raam BJ, Salvesen GS. Proliferative versus apoptotic functions of caspase-8 Hetero or homo: the caspase-8 dimer controls cell fate. Biochim Biophys Acta. 2012; 1824: 113-22.
99. Watanabe Y, Akaike T. Possible involvement of caspase-like family in maintenance of cytoskeleton integrity. J Cell Physiol. 1999; 179: 45-51.
100. Antonopoulos C, Cumberbatch M, Dearman RJ, et al. Functional caspase-1 is required for Langerhans cell migration and optimal contact sensitization in mice. J Immunol. 2001; 166: 3672-7.
101. Helfer B, Boswell BC, Finlay D, et al. Caspase-8 promotes cell motility and calpain activity under nonapoptotic conditions. Cancer Res. 2006; 66: 4273-8.
102. Warso MA, Maniotis AJ, Chen X, et al. Prognostic significance of periodic acid-Schiff-positive patterns in primary cutaneous melanoma. Clin Cancer Res. 2001; 7: 473-7.
103. Thies A, Mangold U, Moll I, et al. PAS-positive loops and networks as a prognostic indicator in cutaneous malignant melanoma. J Pathol. 2001; 195: 537-42.
104. Van Beurden A, Schmitz RF, van Dijk CM, et al. Periodic acid Schiff loops and blood lakes associated with metastasis in cutaneous melanoma. Melanoma Res. 2012; 22: 424-9.
105. Woenckhaus C, Giebel J, Failing K, et al. Expression of AP-2alpha, c-kit, and cleaved caspase-6 and -3 in naevi and malignant melanomas of the skin. A possible role for caspases in melanoma progression? J Pathol. 2003; 201: 278-87.
106. Liu YR, Sun B, Zhao XL, et al. Basal caspase-3 activity promotes migration, invasion, and vasculogenic mimicry formation of melanoma cells. Melanoma Res. 2013; 23: 243-53.
107. Chen K, Zhao H, Hu Z, et al. CASP3 polymorphisms and risk of squamous cell carcinoma of the head and neck. Clin Cancer Res. 2008; 14: 6343-9.
108. Soung YH, Lee JW, Kim SY, et al. Somatic mutations of CASP3 gene in human cancers. Hum Genet. 2004; 115: 112-5.
109. Spinella F, Caprara V, Di Castro V, et al. Endothelin-1 induces the transactivation of vascular endothelial growth factor receptor-3 and modulates cell migration and vasculogenic mimicry in melanoma cells. J Mol Med. 2013; 91: 395-405.
110. Rothhammer T, Bataille F, Spruss T, et al. Functional implication of BMP4 expression on angiogenesis in malignant melanoma. Oncogene. 2007; 26: 4158-70.
111. Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994; 367: 645-8.
112. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003; 100: 3983-8.
113. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004; 432: 396-401.
114. O'Brien CA, Pollett A, Gallinger S, et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007; 445: 106-10.
115. Fang D, Nguyen TK, Leishear K, et al. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 2005; 65: 9328-37.
116. Schatton T, Murphy GF, Frank NY, et al. Identification of cells initiating human melanomas. Nature. 2008; 451: 345-9.
117. Bapat SA, Mali AM, Koppikar CB, et al. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res. 2005; 65: 3025-9.
118. Alvero AB, Chen R, Fu HH, et al. Molecular phenotyping of human ovarian cancer stem cells unravel the mechanisms for repair and chemo-resistance. Cell Cycle. 2009; 8: 158-66.
119. Collins AT, Berry PA, Hyde C, et al. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005; 65: 10946-51.
120. Hermann P, Huber S, Herrler T, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007; 1: 313-23.
121. Ricci-Vitiani L, Pallini R, Biffoni M, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature. 2010; 468: 824-8.
122. Wang R, Chadalavada K, Wilshire J, et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010; 468: 829-33.
123. Charafe-Jauffret E, Ginestier C, Iovino F, et al. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res. 2010; 16: 45-55.
124. Davis SJ, Divi V, Owen JH, et al. Metastatic potential of cancer stem cells in head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg. 2010; 136: 1260-6.
125. Goldie SJ, Mulder KW, Tan DW, et al. FRMD4A upregulation in human squamous cell carcinoma promotes tumor growth and metastasis and is associated with poor prognosis. Cancer Res. 2012; 72: 3424-36.
126. Mirshahi P, Rafii A, Vincent L, et al. Vasculogenic mimicry of acute leukemic bone marrow stromal cells. Leukemia. 2009; 23: 1039-48.
127. Shirakawa K, Wakasugi H, Heike Y, et al. Vasculogenic mimicry and pseudo-comedo formation in breast cancer. Int J Cancer. 2002; 99: 821-8.
128. Yang J, Mani SA, Donaher JL, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004; 117: 927-39.
129. Zhao XL, Sun T, Che N, et al. Promotion of hepatocellular carcinoma metastasis through matrix metalloproteinase activation by epithelial-mesenchymal transition regulator Twist1. J Cell Mol Med. 2011; 15: 691-700.
130. Batlle E, Sancho E, Franci C, et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol. 2000; 2: 84-9.
131. Zhang J, Liang Q, Lei Y, et al. SOX4 induces epithelial-mesenchymal transition and contributes to breast cancer progression. Cancer Res. 2012; 72: 4597-608.
132. Guaita S, Puig I, Franci C, et al. Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J Biol Chem. 2002; 277: 39209-16.
133. Lirdprapamongkol K, Chiablaem K, Sila-Asna M, et al. Exploring stemness gene expression and vasculogenic mimicry capacity in well-and poorly-differentiated hepatocellular carcinoma cell lines. Biochem Biophys Res Commun. 2012; 422: 429-35.
134. Liu Z, Sun B, Qi L, et al. Zinc finger E-box binding homeobox 1 promotes vasculogenic mimicry in colorectal cancer through induction of epithelial-to-mesenchymal transition. Cancer Sci. 2012; 103: 813-20.
135. Xia H, Cheung WK, Sze J, et al. miR-200a regulates epithelial-mesenchymal to stem-like transition via ZEB2 and beta-catenin signaling. J Biol Chem. 2010; 285: 36995-7004.
136. Fang X, Cai Y, Liu J, et al. Twist2 contributes to breast cancer progression by promoting an epithelial-mesenchymal transition and cancer stem-like cell self-renewal. Oncogene. 2011; 30: 4707-20.
137. Santisteban M, Reiman JM, Asiedu MK, et al. Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res. 2009; 69: 2887-95.
138. Mani SA, Guo W, Liao MJ, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008; 133: 704-15.
139. Chen YC, Chen YW, Hsu HS, et al. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun. 2009; 385: 307-13.
140. Sarkar D, Shields B, Davies ML, et al. BRACHYURY confers cancer stem cell characteristics on colorectal cancer cells. Int J Cancer. 2012; 130: 328-37.
141. Zhang S, Li M, Gu Y, et al. Thalidomide influences growth and vasculogenic mimicry channel formation in melanoma. J Exp Clin Cancer Res. 2008; 27: 60.
142. Fu D, He X, Yang S, et al. Zoledronic acid inhibits vasculogenic mimicry in murine osteosarcoma cell line in vitro. BMC Musculoskelet Disord. 2011; 12: 146.
143. Seftor EA, Meltzer PS, Kirschmann DA, et al. Molecular determinants of human uveal melanoma invasion and metastasis. Clin Exp Metastasis. 2002; 19: 233-46.
144. Basu GD, Pathangey LB, Tinder TL, et al. Mechanisms underlying the growth inhibitory effects of the cyclo-oxygenase-2 inhibitor celecoxib in human breast cancer cells. Breast Cancer Res. 2005; 7: R422-35.
145. Itzhaki O, Greenberg E, Shalmon B, et al. Nicotinamide inhibits vasculogenic mimicry, an alternative vascularization pathway observed in highly aggressive melanoma. PLoS ONE. 2013; 8: e57160.
146. Yadav VR, Aggarwal BB. Curcumin: a component of the golden spice, targets multiple angiogenic pathways. Cancer Biol Ther. 2011; 11: 1-6.
147. Baeten CI, Hillen F, Pauwels P, et al. Prognostic role of vasculogenic mimicry in colorectal cancer. Dis Colon Rectum. 2009; 52: 2028-35.
148. Cao Z, Bao M, Miele L, et al. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer. 2013; 49: 3914-23.
149. Lin P, Wang W, Sun BC, et al. Vasculogenic mimicry is a key prognostic factor for laryngeal squamous cell carcinoma: a new pattern of blood supply. Chin Med J. 2012; 125: 3445-9.
150. Sun Q, Zou X, Zhang T, et al. The role of miR-200a in vasculogenic mimicry and its clinical significance in ovarian cancer. Gynecol Oncol. 2014; 132: 730-8.
151. Wang SY, Ke YQ, Lu GH, et al. Vasculogenic mimicry is a prognostic factor for postoperative survival in patients with glioblastoma. J Neurooncol. 2013; 112: 339-45.
152. Massi D, Franchi A, Paglierani M, et al. Vasculogenic mimicry has no prognostic significance in pT3 and pT4 cutaneous melanoma. Hum Pathol. 2004; 35: 496-502.
153. Pignataro L, Carboni N, Midolo V, et al. Clinical relevance of microvessel density in laryngeal squamous cell carcinomas. Int J Cancer. 2001; 92: 666-70.