Vasculogenic mimicry in carcinogenesis and clinical applications

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Abstract

Distinct from classical tumor angiogenesis, vasculogenic mimicry (VM) provides a blood supply for tumor cells independent of endothelial cells. VM has two distinct types, namely tubular type and patterned matrix type. VM is associated with high tumor grade, tumor progression, invasion, metastasis, and poor prognosis in patients with malignant tumors. Herein, we discuss the recent studies on the role of VM in tumor progression and the diverse mechanisms and signaling pathways that regulate VM in tumors. Furthermore, we also summarize the latest findings of non-coding RNAs, such as lncRNAs and miRNAs in VM formation. In addition, we review application of molecular imaging technologies in detection of VM in malignant tumors. Increasing evidence suggests that VM is significantly associated with poor overall survival in patients with malignant tumors and could be a potential therapeutic target.

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Most cited references 97

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Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry.

A J Maniotis, R Folberg, A Hess … (1999)

Tissue sections from aggressive human intraocular (uveal) and metastatic cutaneous melanomas generally lack evidence of significant necrosis and contain patterned networks of interconnected loops of extracellular matrix. The matrix that forms these loops or networks may be solid or hollow. Red blood cells have been detected within the hollow channel components of this patterned matrix histologically, and these vascular channel networks have been detected in human tumors angiographically. Endothelial cells were not identified within these matrix-embedded channels by light microscopy, by transmission electron microscopy, or by using an immunohistochemical panel of endothelial cell markers (Factor VIII-related antigen, Ulex, CD31, CD34, and KDR[Flk-1]). Highly invasive primary and metastatic human melanoma cells formed patterned solid and hollow matrix channels (seen in tissue sections of aggressive primary and metastatic human melanomas) in three-dimensional cultures containing Matrigel or dilute Type I collagen, without endothelial cells or fibroblasts. These tumor cell-generated patterned channels conducted dye, highlighting looping patterns visualized angiographically in human tumors. Neither normal melanocytes nor poorly invasive melanoma cells generated these patterned channels in vitro under identical culture conditions, even after the addition of conditioned medium from metastatic pattern-forming melanoma cells, soluble growth factors, or regimes of hypoxia. Highly invasive and metastatic human melanoma cells, but not poorly invasive melanoma cells, contracted and remodeled floating hydrated gels, providing a biomechanical explanation for the generation of microvessels in vitro. cDNA microarray analysis of highly invasive versus poorly invasive melanoma tumor cells confirmed a genetic reversion to a pluripotent embryonic-like genotype in the highly aggressive melanoma cells. These observations strongly suggest that aggressive melanoma cells may generate vascular channels that facilitate tumor perfusion independent of tumor angiogenesis.

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Expression and functional significance of Twist1 in hepatocellular carcinoma: its role in vasculogenic mimicry.

Tao Sun, Nan Zhao, Xiu-Lan Zhao … (2010)

The up-regulation and nuclear relocation of epithelial-mesenchymal transition (EMT) regulator Twist1 have been implicated in the tumor invasion and metastasis of human hepatocellular carcinoma (HCC). The term vasculogenic mimicry (VM) refers to the unique capability of aggressive tumor cells to mimic the pattern of embryonic vasculogenic networks. However, the relationship between Twist1 and VM formation is not clear. In this study, we explored HCC as a VM and EMT model in order to investigate the role of Twist1 in VM formation. We first examined the expression of Twist1 in human HCC samples and cell lines and found that Twist1 was frequently overexpressed in the nuclear relocation occurring in VM-positive HCCs (13/18 [72%]). Twist1 nuclear expression was likewise significantly associated with VM formation. Clinicopathological analysis revealed that both VM and Twist1 nuclear expressions present shorter survival durations than those without expression. We consistently demonstrated that an overexpression of Twist1 significantly enhanced cell motility, invasiveness, and VM formation in an HepG2 cell. Conversely, a knockdown of Twist1 by the short hairpin RNA approach remarkably reduced Bel7402 cell migration, invasion, and VM formation. Using chromatin immunoprecipitation, we also showed that Twist1 binds to the vascular endothelial (VE)-cadherin promoter and enhances its activity in a transactivation assay. The results of this study indicate that Twist1 induces HCC cell plasticity in VM cells more through the suppression of E-cadherin expression and the induction of VE-cadherin up-regulation than through the VM pattern in vivo and in a three-dimensional in vitro system. Our findings also demonstrate a novel cogitation in cancer stem-like cell differentiation and that related molecular pathways may be used as novel therapeutic targets for the inhibition of HCC angiogenesis and metastasis.

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A new alternative mechanism in glioblastoma vascularization: tubular vasculogenic mimicry.

Soufiane El Hallani, Carole Colin, Marc Sanson … (2010)

Glioblastoma is one of the most angiogenic human tumours and endothelial proliferation is a hallmark of the disease. A better understanding of glioblastoma vasculature is needed to optimize anti-angiogenic therapy that has shown a high but transient efficacy. We analysed human glioblastoma tissues and found non-endothelial cell-lined blood vessels that were formed by tumour cells (vasculogenic mimicry of the tubular type). We hypothesized that CD133+ glioblastoma cells presenting stem-cell properties may express pro-vascular molecules allowing them to form blood vessels de novo. We demonstrated in vitro that glioblastoma stem-like cells were capable of vasculogenesis and endothelium-associated genes expression. Moreover, a fraction of these glioblastoma stem-like cells could transdifferentiate into vascular smooth muscle-like cells. We describe here a new mechanism of alternative glioblastoma vascularization and open a new perspective for the antivascular treatment strategy.

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Author and article information

Contributors

Qingxi Luo: 1005019391@qq.com

Jun Wang: 768735234@qq.com

Wenyuan Zhao: lavandulae@126.com

Zhenzi Peng: 310293830@qq.com

Xianyu Liu: 363123831@qq.com

Bin Li: Ib93036@qq.com

Heng Zhang: 35259928@qq.com

Bin Shan: bin.shan@wsu.edu

Chunfang Zhang: zcf6169@outlook.com

Chaojun Duan: duancjxy@126.com

Journal

Journal ID (nlm-ta): J Hematol Oncol

Journal ID (iso-abbrev): J Hematol Oncol

Title: Journal of Hematology & Oncology

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-8722

Publication date (Electronic): 14 March 2020

Publication date PMC-release: 14 March 2020

Publication date Collection: 2020

Volume: 13

Electronic Location Identifier: 19

Affiliations

[1 ]GRID grid.452223.0, ISNI 0000 0004 1757 7615, Department of Thoracic Surgery, , Xiangya Hospital, Central South University, ; Xiangya Road 87th, Changsha, 410008 Hunan People’s Republic of China

[2 ]GRID grid.452223.0, ISNI 0000 0004 1757 7615, Department of Oncology, National Clinical Research Center for Geriatric Disorders, , Xiangya Hospital, Central South University, ; Changsha, 410008 People’s Republic of China

[3 ]GRID grid.470982.0, ISNI 0000 0004 0400 6231, College of Medicine, , Washington State University Spokane, ; Spokane, WA 99201 USA

Article

Publisher ID: 858

DOI: 10.1186/s13045-020-00858-6

PMC ID: 7071697

PubMed ID: 32169087

SO-VID: 1dcfb7be-4c27-4350-9b44-d50497ce8dfa

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 17 October 2019

Date accepted : 5 March 2020

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 81572281

Award ID: 81974367

Award ID: 81702278

Award Recipient : Chaojun Duan

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: vasculogenic mimicry,cancer,mechanisms,molecular imaging technologies,tumor therapy

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: vasculogenic mimicry, cancer, mechanisms, molecular imaging technologies, tumor therapy

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Vasculogenic mimicry in carcinogenesis and clinical applications

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Karger: Oncology

Most cited references 97

Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry.

Expression and functional significance of Twist1 in hepatocellular carcinoma: its role in vasculogenic mimicry.

A new alternative mechanism in glioblastoma vascularization: tubular vasculogenic mimicry.

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