Vasculogenic mimicry in tumors – current state of the issue
pdf (Русский)

Keywords

vasculogenic mimicry
vasculogenesis
angiogenesis
prognostic role
tumor growth
metastatic spreading

How to Cite

Mnikhovich, M., Bezuglova, T., Erofeeva, L., Romanov, A., Bunkov, K., & Zоrin S. (2022). Vasculogenic mimicry in tumors – current state of the issue. Voprosy Onkologii, 68(6), 700–707. https://doi.org/10.37469/0507-3758-2022-68-6-700-707

Abstract

In the course of evolution, malignant neoplasms acquired various mechanisms aimed at accelerating growth and increasing the probability of metastatic spreading. One of such mechanisms is vasculogenic mimicry maintaining transportation of plasma and formed elements of red blood, bypassing the classical pathways of tumor angiogenesis.

 

Aim. The purpose of the research is to examine the molecular mechanisms and features of the microscopic picture of vasculogenic mimicry, and to identify its role in the tumor process.

Material and Methods. A retrospective analysis of 50 Russian and foreign scientific and clinical studies, as well as review articles on vasculogenic mimicry has been performed.

Conclusion. Determining the role and exact mechanisms of vasculogenic mimicry in carcinogenesis will allow us to develop a set of preventive and therapeutic measures aimed at regressing tumor growth and preventing early metastasis.

https://doi.org/10.37469/0507-3758-2022-68-6-700-707
pdf (Русский)

References

Mueller AJ, Freeman WR, Folberg R et al. Evaluation of microvascularization pattern visibility in humanchoroidal melanomas: comparison of confocal fluorescein with indocyanine green angiography // GraefesArch Clin Exp Ophthalmol. 1999;237:448–56. doi:https://doi.org/10.1007/s004170050260

McDonald DM, Lance Munn, Rakesh KJ. Vasculogenic Mimicry: How Convincing, How Novel, and How Significant? // American Journal of Pathology. 2000;156(2):383–8. doi:10.1016/S0002-9440(10)64740-2

Mueller AJ, Bartsch DU, Folberg R et al. Imaging the microvasculature of choroidal melanomas with con-focal indocyanine green scanning laser ophthalmoscopy // Arch Ophthalmol. 1998;116:31–9.33. doi:10.1001/archopht.116.1.31

Mei X et al. Glioblastoma stem cell differentiation into endothelial cells evidenced through live-cell imaging // Neuro Oncol. 2017;19(8):1109–1118. doi:https://doi.org/10.1093/neuonc/nox016

Bussolati B et al. Endothelial cell differentiation of human breast tumour stem/progenitor cells // J Cell Mol Med. 2009;13(2):309–319. doi:https://doi.org/10.1111/j.1582-4934.2008.00338.x

Folkman J. New perspectives in clinical oncology from angiogenesis research // Eur. J. Cancer. 1996;32A (14):2534–9. doi:https://doi.org/10.1016/S0959-8049(96)00423-6

Easwaran H, Tsai HC, Baylin SB. Cancer epigenetics: tumor heterogeneity, plasticity of stem-like states, and drug resistance // Mol. Cell. 2014;54:716–727. doi:10.1016/j.molcel.2014.05.015. PMID: 24905005

Vempati P, Popel AS, MacGabhann S. Extracellular regulation of VEGF: isoforms, proteolysis, and vascular patterning // Cytokine Growth Factor Rev. 2014;25(1):1–19. doi:https://doi.org/10.1016/j.cytogfr.2013.11.002

De Falco S. The discovery of placenta growth factor and its biological activity // Exp. Mol. Med. 2012;44(1):1–9. doi:https://doi.org/10.3858/emm.2012.44.1.025

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. doi:https://doi.org/10.1158/1078-0432.CCR-11-0659

Fagiani E, Christofori G. Angiopoietins in angiogenesis // Cancer Lett. 2013;328(1):18–26. doi:https://doi.org/10.1016/j.canlet.2012.08.018

Moschetta M, Mishima Y, Sahin I et al. Role of endothelial progenitor cells in cancer progression // Biochim. Biophys. Acta. 2014;1846(1):26–39. doi:https://doi.org/10.1016/j.bbcan.2014.03.005

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. doi:https://doi.org/10.1002/cam4.105

Taha Azad, Mina Ghahremani, Xiaolong Yang. The Role of YAP and TAZ in Angiogenesis and Vascular Mimicry; 2019 May;8(5):407. doi:10.3390/cells8050407

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(3):739–52. doi:10.1016/S0002-9440(10)65173-5. PMID:10487832.

Hendrix MJ, Seftor EA, Hess AR et al. Molecular plasticity of human melanoma cells // Oncogene. 2003;22(20):3070–5.

Григорьева И.Н., Харатишвили Т.К., Барышников А.Ю. Васкулогенная мимикрия: альтернативный механизм кровоснабжения опухоли? // Российский биотерапевтический журнал. 2011;10(3):25–30. EDN QAZQAH. [Grigorieva IN, Kharatishvili TK, Baryshnikov AYu. An alternative mechanism in tumor vascularization: vasculogenic mimicry // Russian Biotherapeutic Journal. 2011;10(3):25–30 (In Russ.)].

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(2):228–33. doi:https://doi.org/10.4161/cbt.5.2.2510

Mourad-Zeidan AA, Melnikova VO, 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. doi:https://doi.org/10.2353/ajpath.2008.080380

Basu GD, Pathangey LB, Tinder TL. 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. doi:https://doi.org/10.1186/bcr1019

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. doi:https://doi.org/10.1007/s10238-012-0190-9

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. doi:https://doi.org/10.1111/j.1549-8719.2011.00102.x

Vartanian A, Stepanova E, Grigorieva I. VEGFR1 and PKC signaling control melanoma vasculogenic mimicry in a VEGFR2 kinase-independent manner // Melanoma Res. 2011;21(2):91–8. doi:10.1097/CMR.0b013e328343a237

Lissitzky JC, 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. doi:https://doi.org/10.1158/0008-5472.CAN-08-2391

Hess AR, Hendrix MJ. Focal adhesion kinase signaling and the aggressive melanoma phenotype // Cell Cycle. 2006;5(5):478–80. doi:https://doi.org/10.4161/cc.5.5.2518

Вартанян А.А. Альтернативное кровоснабжение в костном мозге при онкогематологических заболеваниях // Клин. онкогематол. 2014;7(4):491–500 [Vartanyan AA. Supplemental blood circulation system in hematologic malignancies // Clin. Oncohematol. 2014;7(4):491–500 (In Russ.)].

Semenza GL, Nejfelt MK, Chi SM, Antonarakis SE. Hypoxia-inducible nuclear factors bind to an enhancer element located 3′ to the human erythropoietin gene // Proc Natl Acad Sci US A. 1991;88(13):5680–4. doi:10.1073/pnas.88.13.5680. PMID:2062846.

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. PMID:16997457.

Zhou TJ, Huang XH, Gong L, Xiang L. Vasculogenic mimicry and hypoxia-inducible factor-1alpha expression in cervical squamous cell carcinoma // Genet Mol. Res. 2016 Mar 4;15(1):15017396. doi:10.4238/gmr.15017396. PMID:26985936.

Liu K, Sun B, Zhao X et al. Hypoxia induced epithelial-mesenchymal transition and vasculogenic mimicry formation by promoting Bcl-2/Twist1 cooperation // Exp Mol Pathol. 2015;99(2):383–91. doi:10.1016/j.yexmp.2015.08.009. PMID:26318343.

Sun W, Shen Z, Zhang H et al. Overexpression of HIF-1alpha 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. PMID:22470047.

Seftor RE, Hess AR, Seftor EA et al. Tumor cell vasculogenic mimicry: from controversy to therapeutic promise // Am. J. Pathol. 2012;181(4):1115–1125. doi:10.1016/j.ajpath.2012.07.013. PMID:22944600.

Wegenblast E, Soto M, Gutierrez-Angel S et al. A model of breast cancer heterogeneity reveals vascular mimicry as a driver of metastasis // Nature. 2015;520:358–362. doi:10.1038/nature14403. PMID:25855289.

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. 10.4161 / cbt.5.2.2510 doi:https://doi.org/10.4161/cbt.5.2.2510

Hess AR, Postovit L-M, Margaryan NV et al. Focal adhesion kinase promotes the aggressive melanoma phenotype // Cancer Res. 2005;65:9851–60. doi:https://doi.org/10.1158/0008-5472.CAN-05-2172

Liu W, Xu G, Jia W et al. Prognostic significance and mechanisms of patterned matrix vasculogenic mimicry in hepatocellular carcinoma // Med Oncol. 2011;28 (Suppl. 1):S228–38. doi:10.1007/s12032-010-9706-x

Giannelli G, Falk-Marzillier J, Schiraldi O et al. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5 // Science. 1997;277:225–8. doi:10.1126/science.277.5323.225

Koshikawa N, Giannelli G, Cirulli V et al. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5 // J Cell Biol. 2000;148:615–24. doi:10.1083/jcb.148.3.615

Клеточные линии меланомы человека. Монография / Под общ. ред. И.Н. Михайловой, М.М.Давыдова. СПб.: Наукоемкие технологии, 2017. ISBN: 978-5-9909412-3-6 [Human melanoma cell lines. Monograph / Ed. by N. Mikhailova, M.M. Davydov. St. Petersburg: Science-intensive Technologies, 2017. ISBN:978-5-9909412-3-6 (In Russ.)].

Vartanian A, Gatsina G, Grigorieva I et al. The involvement of Notch signaling in melanoma vasculogenic mimicry // Clin Exp Med. 2013;13:201–209. https://doi.org/10.1007/s10238-012-0190-9

Clarijs R, van Dijk M, Ruiter DJ, de Waal RM. Functional and morphologic analysis of the fluid-conducting meshwork in xenografted cutaneous and primary uveal melanoma // Invest. Ophthalmol. Vis. Sci. 2015;46(9):3013–20. doi:10.1167/iovs.04-0876. PMID:16123395

Foss AJE, Alexander RA, Hungerford J et al. Re-assessment of the PAS patterns in uveal melanoma //Br J Ophthalmol. 1997;81:240–6. doi:http://dx.doi.org/10.1136/bjo.81.3.240

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. doi:https://doi.org/10.1016/S0161-6420(93)31470-3

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(9):1389–98. doi:https://doi.org/10.1016/S0161-6420(93)31470-3

Григорьева И.Н., Харатишвили Т.К., Барышников А.Ю. Васкулогенная мимикрия: альтернативный механизм кровоснабжения опухоли? Российский биотерапевтический журнал. 2011;10(3):25-30 [Grigorieva I.N., Kharatishvili T.K., Baryshnikov A.Yu. Vasculogenic mimicry: an alternative mechanism of tumor blood supply? Russian Biotherapeutic Journal. 2011;10(3):25-30].

Ren K, Yao N, Wang G et al. Vasculogenic mimicry: a new prognostic sign of human osteosarcoma // Hum. Pathol. 2014;45(10):2120–2129. doi:https://doi.org/10.1016/j.humpath.2014.06.013

Liang J, Yang B, Cao Q, Wu X. Association of Vasculogenic Mimicry Formation and CD133 Expression with Poor Prognosis in Ovarian Cancer // Gynecol Obstet Investig. 2016;81(6):529–536. doi:https://doi.org/10.1159/000445747

Li M, Gu Y, Zhang Z et al. Vasculogenic mimicry: a new prognostic sign of gastric adenocarcinoma // Pathol Oncol Res. 2010;16(2):259–266. doi:https://doi.org/10.1007/s12253-009-9220-7

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;29:60. doi:https://doi.org/10.1186/1756-9966-29-60

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 doi:https://doi.org/10.1016/S1470-2045(13)70335-8

Corrie PG, Marshall A, Dunn JA 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. DJI:https://doi.org/10.1016/S1470-2045(14)70110-X

Angara K, Rashid MH, Shankar A et al. Vascular mimicry in glioblastoma following anti-angiogenic and anti-20-HETE therapies // Histol Histopathol. 2016:11856. doi:10.14670/HH-11-856

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

© АННМО «Вопросы онкологии», Copyright (c) 2022