Баланс между обманом и адаптацией: васкулогенная мимикрия как стратегия выживания опухоли
https://doi.org/10.17650/2313-805X-2025-12-1-14-30
Аннотация
Васкулогенная мимикрия представляет собой уникальный процесс, при котором опухолевые клетки имитируют нормальные эндотелиальные клетки сосудов с целью обеспечения себе доступа к кровоснабжению. В настоящем обзоре рассмотрены молекулярные механизмы, предшествующие этому явлению, а также его важность в контексте развития солидных опухолей. Мы проанализировали стратегии выживания опухолевых клеток, использующих васкулогенную мимикрию, и описали потенциальные терапевтические подходы, направленные на подавление роста и метастазирования опухоли. Освещение методов гистологической и молекулярной идентификации васкулогенной мимикрии способствует лучшему пониманию данного феномена и его ранней диагностике. В обзоре акцентируется внимание на необходимости дальнейших исследований васкулогенной мимикрии для формирования представлений о механизмах, лежащих в основе канцерогенеза. Мы проанализировали результаты 109 работ, представленных в ведущих биомедицинских базах данных, включая SciVerse Scopus, PubMed, Web of Science и РИНЦ (Российский индекс научного цитирования), что позволило обобщить актуальные научные данные и выявить ключевые тенденции в области молекулярной онкологии.
Об авторах
Е. А. Просекина
ФГБУ «Национальный медицинский исследовательский центр онкологии им. Н.Н. Петрова» Минздрава России
Россия
Россия
Елизавета Андреевна Просекина
Россия, 197758 Санкт-Петербург, пос. Песочный, ул. Ленинградская, 68
В. А. Шапкина
ФГБОУ ВО «Санкт-Петербургский государственный университет»
Россия
Россия
Россия, 199034 Санкт-Петербург, Университетская наб., 7/9
А. Е. Карпов
ФГБУ «Национальный медицинский исследовательский центр онкологии им. Н.Н. Петрова» Минздрава России
Россия
Россия
Россия, 197758 Санкт-Петербург, пос. Песочный, ул. Ленинградская, 68
Е. Ю. Федоруцева
ФГАОУ ВО «Национальный исследовательский Томский государственный университет»
Россия
Россия
Россия, 634050 Томск, пр-кт Ленина, 36
А. С. Артемьева
ФГБУ «Национальный медицинский исследовательский центр онкологии им. Н.Н. Петрова» Минздрава России
Россия
Россия
Россия, 197758 Санкт-Петербург, пос. Песочный, ул. Ленинградская, 68
Список литературы
1. Kuczynski E.A., Vermeulen P.B., Pezzella F. et al. Vessel co-option in cancer. Nat Rev Clin Oncol 2019;16(8):469–93. DOI: 10.1038/s41571-019-0181-9
2. Jiang X., Wang J., Deng X. et al. The role of microenvironment in tumor angiogenesis. J Exp Clin Cancer Res 2020;39(1):1–19. DOI: 10.1186/s13046-020-01709-5
3. Pinto M.P., Sotomayor P., Carrasco-Avino G. et al. Escaping antiangiogenic therapy: strategies employed by cancer cells. Int J Mol Sci 2016;17(9):1–20. DOI: 10.3390/ijms17091489
4. 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. DOI: 10.1016/S0002-9440(10)65173-5
5. Damsky C.H., Fisher S.J. Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors. Curr Opin Cell Biol 1998;10(5):660–6. DOI: 10.1016/S0955-0674(98)80043-4
6. Kučera T., Strilić B., Regener K. et al. Ancestral vascular lumen formation via basal cell surfaces. PLoS One 2009;4(1):e4132. DOI: 10.1371/JOURNAL.PONE.0004132
7. Racordon D., Valdivia A., Mingo G. et al. Structural and functional identification of vasculogenic mimicry in vitro. Sci Rep 2017;7(1):1–12. DOI: 10.1038/s41598-017-07622-w
8. Paulis Y.W.J., Soetekouw P.M.М.B., Verheul H.M.W. et al. Signalling pathways in vasculogenic mimicry. Biochim Bioph Acta 2010;1806(1):18–28. DOI: 10.1016/J.BBCAN.2010.01.001
9. El Hallani S., Boisselier B., Peglion F. et al. A new alternative mechanism in glioblastoma vascularization: tubular vasculogenic mimicry. Brain 2010;133(Pt 4):973. DOI: 10.1093/BRAIN/AWQ044
10. Wang W., Lin P., Han C. et al. Vasculogenic mimicry contributes to lymph node metastasis of laryngeal squamous cell carcinoma. J Exp Clin Cancer Res 2010;29(1):60. DOI: 10.1186/1756-9966-29-60/TABLES/4
11. Ricci-Vitiani L., Lombardi D.G., Pilozzi E. et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2006;445(7123):111–5. DOI: 10.1038/nature05384
12. Ponti D., Costa A., Zaffaroni N. et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005;65(13):5506–11. DOI: 10.1158/0008-5472.CAN-05-0626
13. Liu Z., Li Y., Zhao W. et al. Demonstration of vasculogenic mimicry in astrocytomas and effects of Endostar on U251 cell. Pathol Res Pract 2011;207(10):645–51. DOI: 10.1016/J.PRP.2011.07.012
14. Gao Y., Zhao X.L., Gu Q. et al. Correlation of vasculogenic mimicry with clinicopathologic features and prognosis of ovarian carcinoma. Zhonghua Bing Li Xue Za Zhi 2009;38(9):585–9. (In Chinese). DOI: 10.3760/cma.j.issn.0529-5807.2009.09.003
15. Lim D., Do Y., Kwon B.S. et al. Angiogenesis and vasculogenic mimicry as therapeutic targets in ovarian cancer. BMB Rep 2020;53(6):291. DOI: 10.5483/BMBREP.2020.53.6.060
16. Van Der Schaft D.W.J., Hillen F., Pauwels P. et al. Tumor cell plasticity in Ewing sarcoma, an alternative circulatory system stimulated by hypoxia. Cancer Res 2005;65(24):11520–8. DOI: 10.1158/0008-5472.CAN-05-2468
17. Cesca K., Oliveira E.M. Confocal laser microscopy for VM analysis with DAPI and phalloidin staining. Methods Mol Biol 2022;2514:153–61. DOI: 10.1007/978-1-0716-2403-6_15
18. De Andrade Peixoto M., Marques dos Reis E., Marques Porto L. Cancer cell spheroids as a 3D model for exploring the pathobiology of vasculogenic mimicry. Methods Mol Biol 2022;2514:45–51. DOI: 10.1007/978-1-0716-2403-6_5
19. 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-(1B4M-Gd) 256. Cancer Res 2002;62(3):860–6.
20. Chen L., Zhang S., Li X. et al. A pilot study of vasculogenic mimicry immunohistochemical expression in intraocular melanoma model. Oncol Rep 2009;21(4):989–94. DOI: 10.3892/OR_00000313/HTML
21. Zhang S., Zhang D., Wang Y. et al. Morphologic research of microcirculation patterns in human and animal melanoma. Med Oncol 2005;23(3):403–9. DOI: 10.1385/MO:23:3:403
22. Angara K., Borin T.F., Arbab A.S. Vascular mimicry: a novel neovascularization mechanism driving anti-angiogenic therapy (AAT) resistance in glioblastoma. Transl Oncol 2017;10(4):650–60. DOI: 10.1016/j.tranon.2017.04.007
23. Delgado-Bellido D., Serrano-Saenz S., Fernández-Cortés M. et al. Vasculogenic mimicry signaling revisited: focus on non-vascular VE-cadherin. Mol Cancer 2017;16(1):1–14. DOI: 10.1186/S12943-017-0631-X
24. Clemente M., Pérez-Alenza M.D., Illera J.C. et al. Histological, immunohistological, and ultrastructural description of vasculogenic mimicry in canine mammary cancer. Vet Pathol 2010;47(2):265–74. DOI: 10.1177/0300985809353167
25. Folberg R., Maniotis A.J. Vasculogenic mimicry. APMIS 2004; 112(7–8):508–25. DOI: 10.1111/J.1600-0463.2004.APM11207-0810.X
26. Hendrix M.J.C., Seftor E.A., Hess A.R. et al. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat Rev Cancer 2003;3(6):411–21. DOI: 10.1038/nrc1092
27. Hendrix M.J.C., Seftor E.A., Kirschmann D.A. et al. Remodeling of the microenvironment by aggressive melanoma tumor cells. Ann N Y Acad Sci 2003;995:151–61. DOI: 10.1111/j.1749-6632.2003.tb03218.x
28. Kirschmann D.A., Seftor E.A., Hardy K.M. et al. Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin Cancer Res 2012;18(10):2726–32. DOI: 10.1158/1078-0432.CCR-11-3237
29. 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. DOI: 10.3892/IJO.25.6.1609/HTML
30. McDonald D.M., Munn L., Jain R.K. Vasculogenic mimicry: how convincing, how novel, and how significant? Am J Pathol 2000;156(2):383. DOI: 10.1016/S0002-9440(10)64740-2
31. Huijbers E.J.M., Van Beijnum J.R., Thijssen V.L. et al. Role of the tumor stroma in resistance to anti-angiogenic therapy. Drug Resist Updat 2016;25:26–37. DOI: 10.1016/J.DRUP.2016.02.002
32. Riabov V., Gudima A., Wang N. et al. Role of tumor associated macrophages in tumor angiogenesis and lymphangiogenesis. Front Physiol 2014;5:75. DOI: 10.3389/FPHYS.2014.00075
33. Barnett F.H., Rosenfeld M., Wood M. et al. Macrophages form functional vascular mimicry channels in vivo. Sci Rep 2016;6:36659. DOI: 10.1038/SREP36659
34. Hutchenreuther J., Vincent K., Norley C.R. et al. Activation of cancer-associated fibroblasts is required for tumor neovascularization in a murine model of melanoma. Matrix Biol 2018;74:52–61. DOI: 10.1016/J.MATBIO.2018.06.003
35. Anderberg C., Pietras K. On the origin of cancer-associated fibroblasts. Cell Cycle 2009;8(10):1461–5. DOI: 10.4161/CC.8.10.8557
36. Yu Y., Xiao C.H., Tan L.D. et al. Cancer-associated fibroblasts induce epithelial-mesenchymal transition of breast cancer cells through paracrine TGF-β signalling. Br J Cancer 2014;110(3):724–32. DOI: 10.1038/BJC.2013.768
37. Heldin C.H., Rubin K., Pietras K. et al. High interstitial fluid pressure – an obstacle in cancer therapy. Nat Rev Cancer 2004;4(10): 806–13. DOI: 10.1038/nrc1456
38. Bittner M., Meltzer P., Chen Y. et al. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 2000;406(6795):536–40. DOI: 10.1038/35020115
39. Seftor E.A., Meltzer P.S., Schatteman G.C. et al. Expression of multiple molecular phenotypes by aggressive melanoma tumor cells: role in vasculogenic mimicry. Crit Rev Oncol Hematol 2002;44(1):17–27. DOI: 10.1016/S1040-8428(01)00199-8
40. Seftor E.A., Meltzer P.S., Kirschmann D.A. et al. Molecular determinants of human uveal melanoma invasion and metastasis. Clin Exp Metastasis 2002;19(3):233–46. DOI: 10.1023/A:1015591624171
41. Sun B., Zhang D., Zhao N. et al. Epithelial-to-endothelial transition and cancer stem cells: two cornerstones of vasculogenic mimicry in malignant tumors. Oncotarget 2017;8(18):30502. DOI: 10.18632/ONCOTARGET.8461
42. Velez D.O., Tsui B., Goshia T. et al. 3D collagen architecture induces a conserved migratory and transcriptional response linked to vasculogenic mimicry. Nature Commun 2017;8(1):1–12. DOI: 10.1038/s41467-017-01556-7
43. Li M., Gu Y., Zhang Z. et al. Vasculogenic mimicry: a new prognostic sign of gastric adenocarcinoma. Pathol Oncol Res 2009;16(2):259–66. DOI: 10.1007/S12253-009-9220-7
44. Lu X.S., Sun W., Ge C.Y. et al. Contribution of the PI3K/MMPs/Ln-5γ2 and EphA2/FAK/Paxillin signaling pathways to tumor growth and vasculogenic mimicry of gallbladder carcinomas. Int J Oncol 2013;42(6):2103–115. DOI: 10.3892/IJO.2013.1897/HTML
45. Liu X., He H., Zhang F. et al. m6A methylated EphA2 and VEGFA through IGF2BP2/3 regulation promotes vasculogenic mimicry in colorectal cancer via PI3K/AKT and ERK1/2 signaling. Cell Death Dis 2022;13(5):483. DOI: 10.1038/S41419-022-04950-2
46. Schnegg C.I., Yang M.H., Ghosh S.K. et al. Induction of vasculogenic mimicry overrides VEGF-A silencing and enriches stem-like cancer cells in melanoma. Cancer Res 2015;75(8):1682–90. DOI: 10.1158/0008-5472.CAN-14-1855/651621/AM/INDUCTION-OF-VASCULOGENIC-MIMICRY-OVERRIDES-VEGF-A
47. Valdivia A., Mingo G., Aldana V. et al. Fact or fiction, it is time for a verdict on vasculogenic mimicry? Front Oncol 2019;9:680. DOI: 10.3389/fonc.2019.00680
48. Williamson S.C., Metcalf R.L., Trapani F. et al. Vasculogenic mimicry in small cell lung cancer. Nat Commun 2016;7(1):1–14. DOI: 10.1038/ncomms13322
49. Liu T.J., Sun B.C., Zhao X.L. et al. CD133+ cells with cancer stem cell characteristics associates with vasculogenic mimicry in triple-negative breast cancer. Oncogene 2013;32(5):544–53. DOI: 10.1038/ONC.2012.85
50. Ren K., Yao N., Wang G. et al. Vasculogenic mimicry: a new prognostic sign of human osteosarcoma. Hum Pathol 2014;45(10): 2120–9. DOI: 10.1016/J.HUMPATH.2014.06.013
51. Tang N.N., Zhu H., Zhang H.J. et al. HIF-1α induces VE-cadherin expression and modulates vasculogenic mimicry in esophageal carcinoma cells. World J Gastroenterol 2914;20(47):17894–904. DOI: 10.3748/WJG.V20.I47.17894
52. Xiao T., Zhong W., Zhao J. et al. Polyphyllin I suppresses the formation of vasculogenic mimicry via Twist1/VE-cadherin pathway. Cell Death Dis 2018;9(9):906. DOI: 10.1038/S41419-018-0902-5
53. Yeo C., Lee H.J., Lee E.O. Serum promotes vasculogenic mimicry through the EphA2/VE-cadherin/AKT pathway in PC-3 human prostate cancer cells. Life Sci 2019;221:267–73. DOI: 10.1016/J.LFS.2019.02.043
54. Zhao N., Sun B.C., Sun T. et al. Hypoxia-induced vasculogenic mimicry formation via VE-cadherin regulation by Bcl-2. Med Oncol 2912;29(5):3599–607. DOI: 10.1007/S12032-012-0245-5
55. Chen L.X., He Y.J., Zhao S.Z. et al. Inhibition of tumor growth and vasculogenic mimicry by curcumin through down-regulation of the EphA2/PI3K/MMP pathway in a murine choroidal melanoma model. Cancer Biol Ther 2011;11(2):229–35. DOI: 10.4161/CBT.11.2.13842
56. Hess A.R., Margaryan N.V., Seftor E.A. 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(12):3283–96. DOI: 10.1002/DVDY.21190
57. Margaryan N.V., Strizzi L., Abbott D.E. et al. EphA2 as a promoter of melanoma tumorigenicity. Cancer Biol Ther 2009;8(3):279. DOI: 10.4161/CBT.8.3.7485
58. Hess A.R., Seftor E.A., Seftor R.E.B. 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(16):4757–62.
59. Li Y., Sun B., Zhao X. et al. MMP-2 and MMP-13 affect vasculogenic mimicry formation in large cell lung cancer. J Cell Mol Med 2017;21(12):3741. DOI: 10.1111/JCMM.13283
60. Liu X., Fassett J., Wei Y., Chen Y. Regulation of DDAH1 as a potential therapeutic target for treating cardiovascular diseases. Evid Based Complement Alternat Med 2013;2:2013:619207. DOI: 10.1155/2013/619207
61. Seftor R.E.B., Seftor E.A., 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(17):6322–7.
62. Yodkeeree S., Chaiwangyen W., Garbisa S. et al. Curcumin, demethoxycurcumin and bisdemethoxycurcumin differentially inhibit cancer cell invasion through the down-regulation of MMPs and uPA. J Nutr Biochem 2009;20(2):87–95. DOI: 10.1016/j.jnutbio.2007.12.003
63. Sood A.K., Seftor E.A., Fletcher M.S. et al. Molecular determinants of ovarian cancer plasticity. Am J Pathol 2001;158(4):1279–88. DOI: 10.1016/S0002-9440(10)64079-5
64. Hess A.R., Postovit L.M., Margaryan N.V. et al. Focal adhesion kinase promotes the aggressive melanoma phenotype. Cancer Res 2005;65(21):9851–60. DOI: 10.1158/0008-5472.CAN-05-2172
65. Fu R., Du W., Ding Z. et al. HIF-1α promoted vasculogenic mimicry formation in lung adenocarcinoma through NRP1 upregulation in the hypoxic tumor microenvironment. Cell Death Disease 2021;12(4):1–11. DOI: 10.1038/s41419-021-03682-z
66. Li W., Zong S.Q., Shi Q. et al. Hypoxia-induced vasculogenic mimicry formation in human colorectal cancer cells: involvement of HIF-1α, claudin-4, and E-cadherin and vimentin. Sci Rep 2016;6:37534. DOI: 10.1038/SREP37534
67. Song Y.Y., Sun L.D., Liu M.L. et al. STAT3, p-STAT3 and HIF-1α are associated with vasculogenic mimicry and impact on survival in gastric adenocarcinoma. Oncol Lett 2014;8(1):431–7. DOI: 10.3892/OL.2014.2059
68. Sun W., Shen Z.Y., 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(6): 1990–2002. DOI: 10.3892/OR.2012.1746
69. Wang M., Zhao X., Zhu D. et al. HIF-1α promoted vasculogenic mimicry formation in hepatocellular carcinoma through LOXL2 up-regulation in hypoxic tumor microenvironment. J Exp Clin Cancer Res 2017;36(1):60. DOI: 10.1186/S13046-017-0533-1
70. Wu S., Cheng Z., Yu L. et al. [Expression of CD82/KAI1 and HIF-1α in non-small cell lung cancer and their relationship to vasculogenic mimicry]. Zhongguo Fei Ai Za Zhi 2011;14(12):918–25. DOI: 10.3779/J.ISSN.1009-3419.2011.12.04
71. Zhang J.G., Zhou H.M., Zhang X. et al. Hypoxic induction of vasculogenic mimicry in hepatocellular carcinoma: role of HIF-1α, RhoA/ROCK and Rac1/PAK signaling. BMC Cancer 2020;20(1):32. DOI: 10.1186/S12885-019-6501-8
72. Wang Y., Yang R., Wang X. et al. Evaluation of the correlation of vasculogenic mimicry, Notch4, DLL4, and KAI1/CD82 in the prediction of metastasis and prognosis in non-small cell lung cancer. Medicine 2018;97(52):e13817. DOI: 10.1097/MD.0000000000013817
73. Strizzi L., Postovit L.M., Margaryan N.V. et al. Nodal as a biomarker for melanoma progression and a new therapeutic target for clinical intervention. Expert Rev Dermatol 2009;4(1):67–78. DOI: 10.1586/17469872.4.1.67
74. Strizzi L., Hardy K.M., Seftor E.A. et al. Development and cancer: At the crossroads of Nodal and Notch signaling. Cancer Res 2009;69(18):7131. DOI: 10.1158/0008-5472.CAN-09-1199
75. Hardy K.M., Kirschmann D.A., Seftor E.A. et al. Regulation of the embryonic morphogen Nodal by Notch4 facilitates manifestation of the aggressive melanoma phenotype. Cancer Res 2010;70(24):10340–50. DOI: 10.1158/0008-5472.CAN-10-0705
76. Gong W., Sun B., Zhao X. et al. Nodal signaling promotes vasculogenic mimicry formation in breast cancer via the Smad2/3 pathway. Oncotarget 2016;7(43):70152. DOI: 10.18632/ONCOTARGET.12161
77. Zang M., Hu L., Zhang B. et al. Luteolin suppresses angiogenesis and vasculogenic mimicry formation through inhibiting Notch1-VEGF signaling in gastric cancer. Biochem Biophys Res Commun 2017;490(3):913–19. DOI: 10.1016/J.BBRC.2017.06.140
78. Hsu M.Y., Yang M.H., Schnegg C.I. et al. Notch3 signaling-mediated melanoma-endothelial crosstalk regulates melanoma stem-like cell homeostasis and niche morphogenesis. Lab Invest 2017;97(6):725–36. DOI: 10.1038/LABINVEST.2017.1
79. Han C., Sun B., Zhao X. et al. Phosphorylation of STAT3 promotes vasculogenic mimicry by inducing epithelial-to-mesenchymal transition in colorectal cancer. Technol Cancer Res Treat 2017;16(6):1209–19. DOI: 10.1177/1533034617742312
80. Sun T., Zhao N., Zhao X.L. et al. Expression and functional significance of Twist1 in hepatocellular carcinoma: its role in vasculogenic mimicry. Hepatology 2010;51(2):545–56. DOI: 10.1002/HEP.23311
81. Hulin J.A., Tommasi S., Elliot D., Mangoni A.A. Small molecule inhibition of DDAH1 significantly attenuates triple negative breast cancer cell vasculogenic mimicry in vitro. Biomed Pharmacother 2019;111:602–12. DOI: 10.1016/j.biopha.2018.12.117
82. Cabral-Pacheco G.A., Garza-Veloz I., Castruita-De la Rosa C. et al. The roles of matrix metalloproteinases and their inhibitors in human diseases. Int J Mol Sci 2020;21(24):1–53. DOI: 10.3390/IJMS21249739
83. Sharma N., Seftor R.E., Seftor E.A. et al. Prostatic tumor cell plasticity involves cooperative interactions of distinct phenotypic subpopulations: role in vasculogenic mimicry. Prostate 2002;50(3):189–201. DOI: 10.1002/PROS.10048
84. Noorolyai S., Shajari N., Baghbani E. et al. The relation between PI3K/AKT signalling pathway and cancer. Gene 2019;698:120–8. DOI: 10.1016/J.GENE.2019.02.076
85. Hendrix M.J.C., Seftor E.A., Meltzer P.S. 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(14):8018–23. DOI: 10.1073/PNAS.131209798
86. Ferrara N. Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am J Physiol Cell Physiol 2001;280(6):49–6. DOI: 10.1152/AJPCELL.2001.280.6.C1358
87. Hanahan D., Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996;86(3):353–64. DOI: 10.1016/S0092-8674(00)80108-7
88. Wang J.Y., Sun T., Zhao X.L. et al. Functional significance of VEGF-a in human ovarian carcinoma: role in vasculogenic mimicry. Cancer Biol Ther 2008;7(5):758–66. DOI: 10.4161/CBT.7.5.5765
89. Cheng N., Brantley D., Fang W.B. et al. Inhibition of VEGF-dependent multistage carcinogenesis by soluble EphA receptors. Neoplasia 2003;5(5):445–56. DOI: 10.1016/S1476-5586(03)80047-7
90. Frank N.Y., Schatton T., Kim S. et al. VEGFR-1 expressed by malignant melanoma-initiating cells is required for tumor growth. Cancer Res 2011;71(4):1474–85. DOI: 10.1158/0008-5472.CAN-10-1660
91. Serova M., Tijeras-Raballand A., Dos Santos C. et al. Everolimus affects vasculogenic mimicry in renal carcinoma resistant to sunitinib. Oncotarget 2016;7(25):38467–86. DOI: 10.18632/ONCOTARGET.9542
92. Sun H., Zhang D., Yao Z. et al. Anti-angiogenic treatment promotes triple-negative breast cancer invasion via vasculogenic mimicry. Cancer Biol Ther 2017;18(4):205–13. DOI: 10.1080/15384047.2017.1294288
93. Brown S., Teo A., Pauklin S. et al. Activin/Nodal signaling controls divergent transcriptional networks in human embryonic stem cells and in endoderm progenitors. Stem Cells 2011;20(8):1176–85. DOI: 10.1002/STEM.666
94. Topczewska J.M., Postovit L.M., Margaryan N.V. et al. Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nat Med 2006;12(8):925–32. DOI: 10.1038/NM1448
95. Jue C., Lin C., Zhisheng Z. et al. Notch1 promotes vasculogenic mimicry in hepatocellular carcinoma by inducing EMT signaling. Oncotarget 2017;8(2):2501. DOI: 10.18632/ONCOTARGET.12388
96. Lee S.L.C., Rouhi P., Dahl Jensen L. et al. Hypoxia-induced pathological angiogenesis mediates tumor cell dissemination, invasion, and metastasis in a zebrafish tumor model. Proc Natl Acad Sci USA 2009;106(46):19485–90. DOI: 10.1073/PNAS.0909228106
97. Wei X., Chen Y., Jiang X. et al. Mechanisms of vasculogenic mimicry in hypoxic tumor microenvironments. Mol Cancer 2021;20(1):1–18. DOI: 10.1186/s12943-020-01288-1
98. De Bock K., Mazzone M., Carmeliet P. Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not? Nat Rev Clin Oncol 2011;8(7):393–404. DOI: 10.1038/NRCLINONC.2011.83
99. Compernolle V., Brusselmans K., Acker T. et al. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 2002;8(7):702–10. DOI: 10.1038/NM721
100. Postovit L.M., Abbott D.E., Payne S.L. et al. Hypoxia/reoxygenation: a dynamic regulator of lysyl oxidase-facilitated breast cancer migration. J Cell Biochem 2008;103(5):1369–78. DOI: 10.1002/jcb.21517
101. Jin-lu M., Han S.X., Zhu Q. et al. Role of Twist in vasculogenic mimicry formation in hypoxic hepatocellular carcinoma cells in vitro. Biochem Biophys Res Commun 2011;408(4):686–91. DOI: 10.1016/J.BBRC.2011.04.089
102. Zhang S., Li M., Zhang D. et al. Hypoxia influences linearly patterned programmed cell necrosis and tumor blood supply patterns formation in melanoma. Lab Invest 2009;89(5):575–86. DOI: 10.1038/LABINVEST.2009.20
103. 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(2):188–97. DOI: 10.1016/J.CANLET.2006.08.016
104. Quail D.F., Taylor M.J., Walsh L.A. et al. Low oxygen levels induce the expression of the embryonic morphogen Nodal. Mol Biol Cell 2011;22(24):4809–21. DOI: 10.1091/MBC.E11-03-0263
105. 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 Cancer Res 2011;30(1):6. DOI: 10.1186/1756-9966-30-6
106. Wu W.K.K., Yiu Sung J.J., Lee C.W. et al. Cyclooxygenase-2 in tumorigenesis of gastrointestinal cancers: an update on the molecular mechanisms. Cancer Lett 2010;295(1):7–16. DOI: 10.1016/J.CANLET.2010.03.015
107. Basu G.D., Liang W.S., Stephan D.A. et al. A novel role for cyclooxygenase-2 in regulating vascular channel formation by human breast cancer cells. Breast Cancer Res 2006;8(6):1–11. DOI: 10.1186/BCR1626/FIGURES/6
108. Rong X., Huang B., Qiu S. et al. Tumor-associated macrophages induce vasculogenic mimicry of glioblastoma multiforme through cyclooxygenase-2 activation. Oncotarget 2016;7(51):83976–86. DOI: 10.18632/ONCOTARGET.6930
Рецензия
Для цитирования:
Просекина Е.А., Шапкина В.А., Карпов А.Е., Федоруцева Е.Ю., Артемьева А.С. Баланс между обманом и адаптацией: васкулогенная мимикрия как стратегия выживания опухоли. Успехи молекулярной онкологии. 2025;12(1):14-30. https://doi.org/10.17650/2313-805X-2025-12-1-14-30
For citation:
Prosekina E.A., Shapkina V.A., Karpov A.E., Fedorutseva E.Yu., Artemyeva A.S. The balance between deception and adaptation: vasculogenic mimicry as a tumor survival strategy. Advances in Molecular Oncology. 2025;12(1):14-30. (In Russ.) https://doi.org/10.17650/2313-805X-2025-12-1-14-30
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