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The emerging roles of circular RNAs in vessel co-option and vasculogenic mimicry: clinical insights for anti-angiogenic therapy in cancers

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Abstract

Unexpected resistance to anti-angiogenic treatment prompted the investigation of non-angiogenic tumor processes. Vessel co-option (VC) and vasculogenic mimicry (VM) are recognized as primary non-angiogenic mechanisms. In VC, cancer cells utilize pre-existing blood vessels for support, whereas in VM, cancer cells channel and provide blood flow to rapidly growing tumors. Both processes have been implicated in the development of tumor and resistance to anti-angiogenic drugs in many tumor types. The morphology, but rare molecular alterations have been investigated in VC and VM. There is a pressing need to better understand the underlying cellular and molecular mechanisms. Here, we review the emerging circular RNA (circRNA)–mediated regulation of non-angiogenic processes, VC and VM.

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Abbreviations

ARP2/3:

Actin-related protein 2/3

BEV:

Bevacizumab

CAMs:

Cell adhesion molecules

CC:

Cervical cancer

CCRCC:

Clear cell renal cell carcinoma

circRNA:

Circular RNA

CRC:

Colorectal cancer

CSC:

Cancer stem cells

CXCL12:

CXC motif chemokine ligand 12

CXCR4:

CXC motif chemokine receptor 4

ECM:

Extracellular matrix

EBV:

Epstein-Barr virus

EMT:

Epithelial-to-mesenchymal transition

EphA2:

Erythropoietin-producing hepatocellular receptor A2

ER:

Endoplasmic reticulum

EVs:

Endothelium-dependent vessels

ERK1/2:

Extracellular signal-regulated kinase 1 and 2

EVMM:

Extravascular migratory metastasis

FAK:

Focal adhesion kinase

GBM:

Glioblastoma

GC:

Gastric cancer

HCC:

Hepatocellular carcinoma

HIF-1α:

Hypoxia-inducible factor-1α

HUVECs:

Human umbilical vein endothelial cells

IL-8:

Interleukin-8

IRE1:

Inositol-requiring enzyme 1

JMY:

Junctional mediating and regulator Y

L1CAM:

L1 cell adhesion molecule

MDM2:

Mouse double minute 2

miRNA:

MicroRNA

MMP2:

Matrix metalloproteinase 2

MV:

Mosaic vessels

NPC:

Nasopharyngeal carcinoma

NSCLC:

Non-small cell lung cancer

OC:

Ovarian cancer

OS:

Overall survival

RCC:

Renal cell carcinoma

SNAIL2:

Transcription factor Slug

THBS1:

Thrombospondin-1

TME:

Tumor microenvironment

TNBC:

Triple-negative breast cancer

VC:

Vessel co-option

VE:

Vascular endothelial

VEGF:

Vascular endothelial growth factor

VEGFR:

VEGF receptors

VM:

Vasculogenic mimicry

References

  1. Hanahan, D., & Weinberg, R. A. (2000). The hallmarks of cancer. Cell, 100(1), 57–70. https://doi.org/10.1016/s0092-8674(00)81683-9

    Article  CAS  PubMed  Google Scholar 

  2. Vasudev, N. S., & Reynolds, A. R. (2014). Anti-angiogenic therapy for cancer: Current progress, unresolved questions and future directions. [; Research Support, Non-U.S. Gov’t Review]. Angiogenesis, 17(3), 471–494. https://doi.org/10.1007/s10456-014-9420-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Jayson, G. C., Kerbel, R., Ellis, L. M., & Harris, A. L. (2016). Antiangiogenic therapy in oncology: Current status and future directions. Lancet, 388(10043), 518–529. https://doi.org/10.1016/s0140-6736(15)01088-0

    Article  CAS  PubMed  Google Scholar 

  4. Cloughesy, T. F., Brenner, A., de Groot, J. F., Butowski, N. A., Zach, L., Campian, J. L., et al. (2020). A randomized controlled phase III study of VB-111 combined with bevacizumab vs bevacizumab monotherapy in patients with recurrent glioblastoma (GLOBE). Neuro-Oncology, 22(5), 705–717. https://doi.org/10.1093/neuonc/noz232

    Article  CAS  PubMed  Google Scholar 

  5. Zeng, Y., & Fu, B. M. (2020). Resistance mechanisms of anti-angiogenic therapy and exosomes-mediated revascularization in cancer. Frontiers in Cell and Developmental Biology, 8, 610661. https://doi.org/10.3389/fcell.2020.610661

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kuczynski, E. A., Vermeulen, P. B., Pezzella, F., Kerbel, R. S., & Reynolds, A. R. (2019). Vessel co-option in cancer. Nature Reviews Clinical Oncology, 16(8), 469–493. https://doi.org/10.1038/s41571-019-0181-9

    Article  CAS  PubMed  Google Scholar 

  7. Zhang, J., Qiao, L., Liang, N., Xie, J., Luo, H., Deng, G., et al. (2016). Vasculogenic mimicry and tumor metastasis. Journal of B.U.ON., 21(3), 533–541.

    PubMed  Google Scholar 

  8. Latacz, E., Caspani, E., Barnhill, R., Lugassy, C., Verhoef, C., Grunhagen, D., et al. (2020). Pathological features of vessel co-option versus sprouting angiogenesis. Angiogenesis, 23(1), 43–54. https://doi.org/10.1007/s10456-019-09690-0

    Article  CAS  PubMed  Google Scholar 

  9. Kuczynski, E. A., & Reynolds, A. R. (2020). Vessel co-option and resistance to anti-angiogenic therapy. Angiogenesis, 23(1), 55–74. https://doi.org/10.1007/s10456-019-09698-6

    Article  CAS  PubMed  Google Scholar 

  10. Fathi Maroufi, N., Taefehshokr, S., Rashidi, M.-R., Taefehshokr, N., Khoshakhlagh, M., Isazadeh, A., et al. (2020). Vascular mimicry: Changing the therapeutic paradigms in cancer. Molecular Biology Reports, 47(6), 4749–4765. https://doi.org/10.1007/s11033-020-05515-2

    Article  CAS  PubMed  Google Scholar 

  11. Kristensen, L. S., Andersen, M. S., Stagsted, L. V. W., Ebbesen, K. K., Hansen, T. B., & Kjems, J. (2019). The biogenesis, biology and characterization of circular RNAs. Nature Reviews Genetics, 20(11), 675–691. https://doi.org/10.1038/s41576-019-0158-7

    Article  CAS  PubMed  Google Scholar 

  12. Shao, Y., Lu, B. (2020). The crosstalk between circular RNAs and the tumor microenvironment in cancer metastasis. Cancer Cell International, 20(1), https://doi.org/10.1186/s12935-020-01532-0

  13. Pezzella, F., Di Bacco, A., Andreola, S., Nicholson, A. G., Pastorino, U., & Harris, A. L. (1996). Angiogenesis in primary lung cancer and lung secondaries. The European Journal of Cancer, 32a(14), 2494–2500. https://doi.org/10.1016/s0959-8049(96)00377-2

    Article  CAS  PubMed  Google Scholar 

  14. Pezzella, F., Pastorino, U., Tagliabue, E., Andreola, S., Sozzi, G., Gasparini, G., et al. (1997). Non-small-cell lung carcinoma tumor growth without morphological evidence of neo-angiogenesis. American Journal of Pathology, 151(5), 1417–1423.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Lugassy, C., Zadran, S., Bentolila, L. A., Wadehra, M., Prakash, R., Carmichael, S. T., et al. (2014). Angiotropism, pericytic mimicry and extravascular migratory metastasis in melanoma: An alternative to intravascular cancer dissemination. Cancer Microenvironment, 7(3), 139–152. https://doi.org/10.1007/s12307-014-0156-4

    Article  PubMed  PubMed Central  Google Scholar 

  16. Baker, G. J., Yadav, V. N., Motsch, S., Koschmann, C., Calinescu, A. A., Mineharu, Y., et al. (2014). Mechanisms of glioma formation: Iterative perivascular glioma growth and invasion leads to tumor progression, VEGF-independent vascularization, and resistance to antiangiogenic therapy. Neoplasia, 16(7), 543–561. https://doi.org/10.1016/j.neo.2014.06.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia (2009). Hepatology, 49(2), 658–664, https://doi.org/10.1002/hep.22709

  18. van Dam, P. J., van der Stok, E. P., Teuwen, L. A., Van den Eynden, G. G., Illemann, M., Frentzas, S., et al. (2017). International consensus guidelines for scoring the histopathological growth patterns of liver metastasis. British Journal of Cancer, 117(10), 1427–1441. https://doi.org/10.1038/bjc.2017.334

    Article  PubMed  PubMed Central  Google Scholar 

  19. Rada, M., Lazaris, A., Kapelanski-Lamoureux, A., Mayer, T. Z., & Metrakos, P. (2020). Tumor microenvironment conditions that favor vessel co-option in colorectal cancer liver metastases: A theoretical model. Seminars in Cancer Biology. https://doi.org/10.1016/j.semcancer.2020.09.001

    Article  PubMed  Google Scholar 

  20. Griveau, A., Seano, G., Shelton, S. J., Kupp, R., Jahangiri, A., Obernier, K., et al. (2018). A glial signature and wnt7 signaling regulate glioma-vascular interactions and tumor microenvironment. Cancer Cell, 33(5), 874-889.e877. https://doi.org/10.1016/j.ccell.2018.03.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kuczynski, E. A., Yin, M., Bar-Zion, A., Lee, C. R., Butz, H., Man, S., et al. (2016). Co-option of liver vessels and not sprouting angiogenesis drives acquired sorafenib resistance in hepatocellular carcinoma. Journal of the National Cancer Institute, 108(8), https://doi.org/10.1093/jnci/djw030

  22. Voutouri, C., Kirkpatrick, N. D., Chung, E., Mpekris, F., Baish, J. W., Munn, L. L., et al. (2019). Experimental and computational analyses reveal dynamics of tumor vessel cooption and optimal treatment strategies. Proceedings of the National Academy of Sciences of the United States of America, 116(7), 2662–2671. https://doi.org/10.1073/pnas.1818322116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bridgeman, V. L., Vermeulen, P. B., Foo, S., Bilecz, A., Daley, F., Kostaras, E., et al. (2017). Vessel co-option is common in human lung metastases and mediates resistance to anti-angiogenic therapy in preclinical lung metastasis models. Journal of Pathology, 241(3), 362–374. https://doi.org/10.1002/path.4845

    Article  CAS  PubMed  Google Scholar 

  24. Dome, B., Timar, J., & Paku, S. (2003). A novel concept of glomeruloid body formation in experimental cerebral metastases. Journal of Neuropathology and Experimental Neurology, 62(6), 655–661.

    Article  PubMed  Google Scholar 

  25. Stessels, F., Van den Eynden, G., Van der Auwera, I., Salgado, R., Van den Heuvel, E., Harris, A. L., et al. (2004). Breast adenocarcinoma liver metastases, in contrast to colorectal cancer liver metastases, display a non-angiogenic growth pattern that preserves the stroma and lacks hypoxia. British Journal of Cancer, 90(7), 1429–1436. https://doi.org/10.1038/sj.bjc.6601727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Vermeulen, P. B., Colpaert, C., Salgado, R., Royers, R., Hellemans, H., Van den Heuvel, E., et al. (2001). Liver metastases from colorectal adenocarcinomas grow in three patterns with different angiogenesis and desmoplasia. Journal of Pathology, 195(3), 336–342. https://doi.org/10.1002/path.966

    Article  CAS  PubMed  Google Scholar 

  27. Kita, K., Itoshima, T., & Tsuji, T. (1991). Observation of microvascular casts of human hepatocellular-carcinoma by scanning electron-microscopy. Gastroenterologia Japonica, 26(3), 319–328.

    Article  CAS  PubMed  Google Scholar 

  28. Ebos, J. M., & Kerbel, R. S. (2011). Antiangiogenic therapy: Impact on invasion, disease progression, and metastasis. Nature Reviews. Clinical Oncology, 8(4), 210–221. https://doi.org/10.1038/nrclinonc.2011.21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Roviello, G., Bachelot, T., Hudis, C. A., Curigliano, G., Reynolds, A. R., Petrioli, R., et al. (2017). The role of bevacizumab in solid tumours: A literature based meta-analysis of randomised trials. European Journal of Cancer, 75, 245–258. https://doi.org/10.1016/j.ejca.2017.01.026

    Article  CAS  PubMed  Google Scholar 

  30. Porta, C., Cosmai, L., Leibovich, B. C., Powles, T., Gallieni, M., & Bex, A. (2019). The adjuvant treatment of kidney cancer: A multidisciplinary outlook. Nature reviews. Nephrology, 15(7), 423–433. https://doi.org/10.1038/s41581-019-0131-x

    Article  PubMed  Google Scholar 

  31. Frentzas, S., Simoneau, E., Bridgeman, V. L., Vermeulen, P. B., Foo, S., Kostaras, E., et al. (2016). Vessel co-option mediates resistance to anti-angiogenic therapy in liver metastases. Nature Medicine, 22(11), 1294–1302. https://doi.org/10.1038/nm.4197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kölsch, V., Charest, P. G., & Firtel, R. A. (2008). The regulation of cell motility and chemotaxis by phospholipid signaling. Journal of Cell Science, 121(Pt 5), 551–559. https://doi.org/10.1242/jcs.023333

    Article  CAS  PubMed  Google Scholar 

  33. Lugassy, C., & Barnhill, R. L. (2007). Angiotropic melanoma and extravascular migratory metastasis: A review. Advances in Anatomic Pathology, 14(3), 195–201. https://doi.org/10.1097/PAP.0b013e31805048d9

    Article  PubMed  Google Scholar 

  34. Watkins, S., Robel, S., Kimbrough, I. F., Robert, S. M., Ellis-Davies, G., & Sontheimer, H. (2014). Disruption of astrocyte-vascular coupling and the blood-brain barrier by invading glioma cells. Nature Communications, 5, 4196. https://doi.org/10.1038/ncomms5196

    Article  CAS  PubMed  Google Scholar 

  35. Kienast, Y., von Baumgarten, L., Fuhrmann, M., Klinkert, W. E., Goldbrunner, R., Herms, J., et al. (2010). Real-time imaging reveals the single steps of brain metastasis formation. Nature Medicine, 16(1), 116–122. https://doi.org/10.1038/nm.2072

    Article  CAS  PubMed  Google Scholar 

  36. Garcia-Gomez, P., & Valiente, M. (2020). Vascular co-option in brain metastasis. Angiogenesis, 23(1), 3–8. https://doi.org/10.1007/s10456-019-09693-x

    Article  PubMed  Google Scholar 

  37. Caspani, E. M., Crossley, P. H., Redondo-Garcia, C., & Martinez, S. (2014). Glioblastoma: A pathogenic crosstalk between tumor cells and pericytes. PLoS ONE, 9(7), e101402. https://doi.org/10.1371/journal.pone.0101402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tse, J. M., Cheng, G., Tyrrell, J. A., Wilcox-Adelman, S. A., Boucher, Y., Jain, R. K., et al. (2012). Mechanical compression drives cancer cells toward invasive phenotype. Proceedings of the National Academy of Sciences of the United States of America, 109(3), 911–916. https://doi.org/10.1073/pnas.1118910109

    Article  PubMed  Google Scholar 

  39. Butler, J. M., Kobayashi, H., & Rafii, S. (2010). Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nature Reviews Cancer, 10(2), 138–146. https://doi.org/10.1038/nrc2791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sharma, I., Singh, A., Siraj, F., & Saxena, S. (2018). IL-8/CXCR1/2 signalling promotes tumor cell proliferation, invasion and vascular mimicry in glioblastoma. Journal of Biomedical Science, 25(1), 62. https://doi.org/10.1186/s12929-018-0464-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Seano, G., & Jain, R. K. (2020). Vessel co-option in glioblastoma: Emerging insights and opportunities. Angiogenesis, 23(1), 9–16. https://doi.org/10.1007/s10456-019-09691-z

    Article  PubMed  Google Scholar 

  42. Pham, K., Luo, D., Siemann, D. W., Law, B. K., Reynolds, B. A., Hothi, P., et al. (2015). VEGFR inhibitors upregulate CXCR4 in VEGF receptor-expressing glioblastoma in a TGFβR signaling-dependent manner. Cancer Letters, 360(1), 60–67. https://doi.org/10.1016/j.canlet.2015.02.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Donnem, T., Reynolds, A. R., Kuczynski, E. A., Gatter, K., Vermeulen, P. B., Kerbel, R. S., et al. (2018). Non-angiogenic tumours and their influence on cancer biology. Nature Reviews Cancer, 18(5), 323–336. https://doi.org/10.1038/nrc.2018.14

    Article  CAS  PubMed  Google Scholar 

  44. Palmieri, V., Lazaris, A., Mayer, T. Z., Petrillo, S. K., Alamri, H., Rada, M., et al. (2020). Neutrophils expressing lysyl oxidase-like 4 protein are present in colorectal cancer liver metastases resistant to anti-angiogenic therapy. The Journal of Pathology, 251(2), 213–223. https://doi.org/10.1002/path.5449

    Article  CAS  PubMed  Google Scholar 

  45. Sun, D., Liu, J., & Zhou, L. (2019). Upregulation of circular RNA circ-FAM53B predicts adverse prognosis and accelerates the progression of ovarian cancer via the miR-646/VAMP2 and miR-647/MDM2 signaling pathways. Oncology Reports, 42(6), 2728–2737. https://doi.org/10.3892/or.2019.7366

    Article  CAS  PubMed  Google Scholar 

  46. Zhang, F., Xu, Y., Ye, W., Jiang, J., & Wu, C. (2020). Circular RNA S-7 promotes ovarian cancer EMT via sponging miR-641 to up-regulate ZEB1 and MDM2. Bioscience Reports, 40(7), https://doi.org/10.1042/BSR20200825

  47. Yanbin, Z., & Jing, Z. (2019). CircSAMD4A accelerates cell proliferation of osteosarcoma by sponging miR-1244 and regulating MDM2 mRNA expression. Biochemical and Biophysical Research Communications, 516(1), 102–111. https://doi.org/10.1016/j.bbrc.2019.05.182

    Article  CAS  PubMed  Google Scholar 

  48. Jin, Y., Li, L., Zhu, T., & Liu, G. (2019). Circular RNA circ_0102049 promotes cell progression as ceRNA to target MDM2 via sponging miR-1304-5p in osteosarcoma. Pathology - Research and Practice, 215(12), 152688. https://doi.org/10.1016/j.prp.2019.152688

    Article  CAS  PubMed  Google Scholar 

  49. Ma, W., Zhao, P., Zang, L., Zhang, K., Liao, H., & Hu, Z. (2020). CircTP53 promotes the proliferation of thyroid cancer via targeting miR-1233-3p/MDM2 axis. Journal of Endocrinological Investigation. https://doi.org/10.1007/s40618-020-01317-2

    Article  PubMed  Google Scholar 

  50. Liu, R., Zhou, M., Zhang, P., Zhao, Y., & Zhang, Y. (2020). Cell proliferation and invasion is promoted by circSERPINA3 in nasopharyngeal carcinoma by regulating miR-944/MDM2 axis. Journal of Cancer, 11(13), 3910–3918. https://doi.org/10.7150/jca.42799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Wang, K., Sun, Y., Tao, W., Fei, X., & Chang, C. (2017). Androgen receptor (AR) promotes clear cell renal cell carcinoma (ccRCC) migration and invasion via altering the circHIAT1/miR-195-5p/29a-3p/29c-3p/CDC42 signals. Cancer Letters, 394, 1–12. https://doi.org/10.1016/j.canlet.2016.12.036

    Article  CAS  PubMed  Google Scholar 

  52. Xing, L., Yang, R., Wang, X., Zheng, X., Yang, X., Zhang, L., et al. (2020). The circRNA circIFI30 promotes progression of triple-negative breast cancer and correlates with prognosis. Aging (Albany NY), 12(11), 10983–11003. https://doi.org/10.18632/aging.103311

    Article  CAS  Google Scholar 

  53. Hong, Y., Qin, H., Li, Y., Zhang, Y., Zhuang, X., Liu, L., et al. (2019). FNDC3B circular RNA promotes the migration and invasion of gastric cancer cells via the regulation of E-cadherin and CD44 expression. Journal of Cellular Physiology, 234(11), 19895–19910. https://doi.org/10.1002/jcp.28588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Ma, H. B., Yao, Y. N., Yu, J. J., Chen, X. X., & Li, H. F. (2018). Extensive profiling of circular RNAs and the potential regulatory role of circRNA-000284 in cell proliferation and invasion of cervical cancer via sponging miR-506. American Journal of Translational Research, 10(2), 592–604.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Du, W. W., Yang, W., Li, X., Fang, L., Wu, N., Li, F., et al. (2020). The circular RNA circSKA3 binds integrin beta1 to induce invadopodium formation enhancing breast cancer invasion. Molecular Therapy, 28(5), 1287–1298. https://doi.org/10.1016/j.ymthe.2020.03.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Yang, W., & Xie, T. (2020). Hsa_circ_CSPP1/MiR-361-5p/ITGB1 regulates proliferation and migration of cervical cancer (CC) by modulating the PI3K-Akt signaling pathway. Reproductive Sciences, 27(1), 132–144. https://doi.org/10.1007/s43032-019-00008-5

    Article  CAS  PubMed  Google Scholar 

  57. Wang, N., Lu, K., Qu, H., Wang, H., Chen, Y., Shan, T., et al. (2020). CircRBM33 regulates IL-6 to promote gastric cancer progression through targeting miR-149. Biomedicine & Pharmacotherapy, 125, 109876. https://doi.org/10.1016/j.biopha.2020.109876

    Article  CAS  Google Scholar 

  58. Xu, Z., Tie, X., Li, N., Yi, Z., Shen, F., & Zhang, Y. (2020). Circular RNA hsa_circ_0000654 promotes esophageal squamous cell carcinoma progression by regulating the miR-149-5p/IL-6/STAT3 pathway. IUBMB Life, 72(3), 426–439. https://doi.org/10.1002/iub.2202

    Article  CAS  PubMed  Google Scholar 

  59. Zhang, P. F., Pei, X., Li, K. S., Jin, L. N., Wang, F., Wu, J., et al. (2019). Circular RNA circFGFR1 promotes progression and anti-PD-1 resistance by sponging miR-381-3p in non-small cell lung cancer cells. Molecular Cancer, 18(1), 179. https://doi.org/10.1186/s12943-019-1111-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Li, H., Yao, G., Feng, B., Lu, X., & Fan, Y. (2018). Circ_0056618 and CXCR4 act as competing endogenous in gastric cancer by regulating miR-206. Journal of Cellular Biochemistry, 119(11), 9543–9551. https://doi.org/10.1002/jcb.27271

    Article  CAS  PubMed  Google Scholar 

  61. Zheng, X., Ma, Y. F., Zhang, X. R., Li, Y., Zhao, H. H., & Han, S. G. (2020). Circ_0056618 promoted cell proliferation, migration and angiogenesis through sponging with miR-206 and upregulating CXCR4 and VEGF-A in colorectal cancer. European Review for Medical and Pharmacological Sciences, 24(8), 4190–4202. https://doi.org/10.26355/eurrev_202004_20999

    Article  CAS  PubMed  Google Scholar 

  62. He, F., Zhong, X., Lin, Z., Lin, J., Qiu, M., Li, X., et al. (2020). Plasma exo-hsa_circRNA_0056616: A potential biomarker for lymph node metastasis in lung adenocarcinoma. Journal of Cancer, 11(14), 4037–4046. https://doi.org/10.7150/jca.30360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Adighibe, O., & Pezzella, F. (2018). The Role of JMY in p53 Regulation. Cancers (Basel), 10(6), https://doi.org/10.3390/cancers10060173

  64. Coutts, A. S., Weston, L., & La Thangue, N. B. (2010). Actin nucleation by a transcription co-factor that links cytoskeletal events with the p53 response. Cell Cycle, 9(8), 1511–1515. https://doi.org/10.4161/cc.9.8.11258

    Article  PubMed  Google Scholar 

  65. Coutts, A. S., Boulahbel, H., Graham, A., & La Thangue, N. B. (2007). Mdm2 targets the p53 transcription cofactor JMY for degradation. EMBO Reports, 8(1), 84–90. https://doi.org/10.1038/sj.embor.7400855

    Article  CAS  PubMed  Google Scholar 

  66. Talme, T., Bergdahl, E., & Sundqvist, K. G. (2014). Regulation of T-lymphocyte motility, adhesion and de-adhesion by a cell surface mechanism directed by low density lipoprotein receptor-related protein 1 and endogenous thrombospondin-1. Immunology, 142(2), 176–192. https://doi.org/10.1111/imm.12229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Daubon, T., Léon, C., Clarke, K., Andrique, L., Salabert, L., Darbo, E., et al. (2019). Deciphering the complex role of thrombospondin-1 in glioblastoma development. Nature Communications, 10(1), 1146. https://doi.org/10.1038/s41467-019-08480-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Skandalis, S. S., Karalis, T. T., Chatzopoulos, A., & Karamanos, N. K. (2019). Hyaluronan-CD44 axis orchestrates cancer stem cell functions. Cellular Signalling, 63, 109377. https://doi.org/10.1016/j.cellsig.2019.109377

    Article  CAS  PubMed  Google Scholar 

  69. Lazaris, A., Amri, A., Petrillo, S. K., Zoroquiain, P., Ibrahim, N., Salman, A., et al. (2018). Vascularization of colorectal carcinoma liver metastasis: Insight into stratification of patients for anti-angiogenic therapies. The Journal of Pathology: Clinical Research, 4(3), 184–192. https://doi.org/10.1002/cjp2.100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Samatov, T. R., Wicklein, D., & Tonevitsky, A. G. (2016). L1CAM: Cell adhesion and more. Progress in Histochemistry and Cytochemistry, 51(2), 25–32. https://doi.org/10.1016/j.proghi.2016.05.001

    Article  PubMed  Google Scholar 

  71. Valiente, M., Obenauf, A. C., Jin, X., Chen, Q., Zhang, X. H., Lee, D. J., et al. (2014). Serpins promote cancer cell survival and vascular co-option in brain metastasis. Cell, 156(5), 1002–1016. https://doi.org/10.1016/j.cell.2014.01.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Er, E. E., Valiente, M., Ganesh, K., Zou, Y., Agrawal, S., Hu, J., et al. (2018). Pericyte-like spreading by disseminated cancer cells activates YAP and MRTF for metastatic colonization. Nature Cell Biology, 20(8), 966–978. https://doi.org/10.1038/s41556-018-0138-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Bugyik, E., Dezso, K., Reiniger, L., László, V., Tóvári, J., Tímár, J., et al. (2011). Lack of angiogenesis in experimental brain metastases. Journal of Neuropathology and Experimental Neurology, 70(11), 979–991. https://doi.org/10.1097/NEN.0b013e318233afd7

    Article  PubMed  Google Scholar 

  74. Yao, H., Price, T. T., Cantelli, G., Ngo, B., Warner, M. J., Olivere, L., et al. (2018). Leukaemia hijacks a neural mechanism to invade the central nervous system. Nature, 560(7716), 55–60. https://doi.org/10.1038/s41586-018-0342-5

    Article  CAS  PubMed  Google Scholar 

  75. Carbonell, W. S., DeLay, M., Jahangiri, A., Park, C. C., & Aghi, M. K. (2013). β1 integrin targeting potentiates antiangiogenic therapy and inhibits the growth of bevacizumab-resistant glioblastoma. Cancer Research, 73(10), 3145–3154. https://doi.org/10.1158/0008-5472.can-13-0011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Chen, D. L., Zeng, Z. L., Yang, J., Ren, C., Wang, D. S., Wu, W. J., et al. (2013). L1cam promotes tumor progression and metastasis and is an independent unfavorable prognostic factor in gastric cancer. Journal of Hematology & Oncology, 6, 43. https://doi.org/10.1186/1756-8722-6-43

    Article  CAS  Google Scholar 

  77. Colombo, F., & Meldolesi, J. (2015). L1-CAM and N-CAM: From adhesion proteins to pharmacological targets. Trends in Pharmacological Sciences, 36(11), 769–781. https://doi.org/10.1016/j.tips.2015.08.004

    Article  CAS  PubMed  Google Scholar 

  78. Carbonell, W. S., Ansorge, O., Sibson, N., & Muschel, R. (2009). The vascular basement membrane as “soil” in brain metastasis. PLoS ONE, 4(6), e5857. https://doi.org/10.1371/journal.pone.0005857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Eddy, R. J., Weidmann, M. D., Sharma, V. P., & Condeelis, J. S. (2017). Tumor Cell Invadopodia: Invasive Protrusions that Orchestrate Metastasis. Trends in Cell Biology, 27(8), 595–607. https://doi.org/10.1016/j.tcb.2017.03.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Lorenz, M., Yamaguchi, H., Wang, Y., Singer, R. H., & Condeelis, J. (2004). Imaging sites of N-wasp activity in lamellipodia and invadopodia of carcinoma cells. Current Biology, 14(8), 697–703. https://doi.org/10.1016/j.cub.2004.04.008

    Article  CAS  PubMed  Google Scholar 

  81. Marx, J. (2006). Cell biology. Podosomes and invadopodia help mobile cells step lively. Science, 312(5782), 1868–1869. https://doi.org/10.1126/science.312.5782.1868

    Article  CAS  PubMed  Google Scholar 

  82. Kumari, N., Dwarakanath, B. S., Das, A., & Bhatt, A. N. (2016). Role of interleukin-6 in cancer progression and therapeutic resistance. Tumour Biology, 37(9), 11553–11572. https://doi.org/10.1007/s13277-016-5098-7

    Article  CAS  PubMed  Google Scholar 

  83. Waugh, D. J., & Wilson, C. (2008). The interleukin-8 pathway in cancer. Clinical Cancer Research, 14(21), 6735–6741. https://doi.org/10.1158/1078-0432.ccr-07-4843

    Article  CAS  PubMed  Google Scholar 

  84. Auf, G., Jabouille, A., Guérit, S., Pineau, R., Delugin, M., Bouchecareilh, M., et al. (2010). Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma. Proceedings of the National Academy of Sciences of the United States of America, 107(35), 15553–15558. https://doi.org/10.1073/pnas.0914072107

    Article  PubMed  PubMed Central  Google Scholar 

  85. Ron, D., & Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nature Reviews Molecular Cell Biology, 8(7), 519–529. https://doi.org/10.1038/nrm2199

    Article  CAS  PubMed  Google Scholar 

  86. Donnem, T., Hu, J., Ferguson, M., Adighibe, O., Snell, C., Harris, A. L., et al. (2013). Vessel co-option in primary human tumors and metastases: An obstacle to effective anti-angiogenic treatment? Cancer Medicine, 2(4), 427–436. https://doi.org/10.1002/cam4.105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Ohe, K., Tanaka, T., Horita, Y., Harada, Y., Yamasaki, T., Abe, I., et al. (2019). Circular IRE-type RNAs of the NR5A1 gene are formed in adrenocortical cells. Biochemical and Biophysical Research Communications, 512(1), 1–6. https://doi.org/10.1016/j.bbrc.2019.02.151

    Article  CAS  PubMed  Google Scholar 

  88. Ruf, W., Seftor, E. A., Petrovan, R. J., Weiss, R. M., Gruman, L. M., Margaryan, N. V., et al. (2003). Differential role of tissue factor pathway inhibitors 1 and 2 in melanoma vasculogenic mimicry. Cancer Research, 63(17), 5381–5389.

    CAS  PubMed  Google Scholar 

  89. Wechman, S. L., Emdad, L., Sarkar, D., Das, S. K., & Fisher, P. B. (2020). Vascular mimicry: Triggers, molecular interactions and in vivo models. Advances in Cancer Research, 148, 27–67. https://doi.org/10.1016/bs.acr.2020.06.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ge, H., & Luo, H. (2018). Overview of advances in vasculogenic mimicry - A potential target for tumor therapy. Cancer Management and Research, 10, 2429–2437. https://doi.org/10.2147/cmar.s164675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Karroum, A., Mirshahi, P., Benabbou, N., Faussat, A. M., Soria, J., Therwath, A., et al. (2010). Matrix metalloproteinase-9 is required for tubular network formation and migration of resistant breast cancer cells MCF-7 through PKC and ERK1/2 signalling pathways. Cancer Letters, 295(2), 242–251. https://doi.org/10.1016/j.canlet.2010.03.007

    Article  CAS  PubMed  Google Scholar 

  92. Lim, D., Do, Y., Kwon, B. S., Chang, W., Lee, M. S., Kim, J., et al. (2020). Angiogenesis and vasculogenic mimicry as therapeutic targets in ovarian cancer. BMB Reports, 53(6), 291–298. https://doi.org/10.5483/BMBRep.2020.53.6.060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Huang, B., Xiao, E., & Huang, M. (2015). MEK/ERK pathway is positively involved in hypoxia-induced vasculogenic mimicry formation in hepatocellular carcinoma which is regulated negatively by protein kinase A. Medical Oncology, 32(1), 408. https://doi.org/10.1007/s12032-014-0408-7

    Article  CAS  PubMed  Google Scholar 

  94. Williamson, S. C., Metcalf, R. L., Trapani, F., Mohan, S., Antonello, J., Abbott, B., et al. (2016). Vasculogenic mimicry in small cell lung cancer. Nature Communications, 7, 13322. https://doi.org/10.1038/ncomms13322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Xu, Y., Li, Q., Li, X. Y., Yang, Q. Y., Xu, W. W., & Liu, G. L. (2012). Short-term anti-vascular endothelial growth factor treatment elicits vasculogenic mimicry formation of tumors to accelerate metastasis. Journal of Experimental & Clinical Cancer Research, 31(1), 16. https://doi.org/10.1186/1756-9966-31-16

    Article  CAS  Google Scholar 

  96. Hu, Y. L., DeLay, M., Jahangiri, A., Molinaro, A. M., Rose, S. D., Carbonell, W. S., et al. (2012). Hypoxia-induced autophagy promotes tumor cell survival and adaptation to antiangiogenic treatment in glioblastoma. Cancer Research, 72(7), 1773–1783. https://doi.org/10.1158/0008-5472.can-11-3831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Angara, K., Borin, T. F., Rashid, M. H., Lebedyeva, I., Ara, R., Lin, P. C., et al. (2018). CXCR2-expressing tumor cells drive vascular mimicry in antiangiogenic therapy-resistant glioblastoma. Neoplasia, 20(10), 1070–1082. https://doi.org/10.1016/j.neo.2018.08.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Liu, R., Yang, K., Meng, C., Zhang, Z., & Xu, Y. (2012). Vasculogenic mimicry is a marker of poor prognosis in prostate cancer. Cancer Biology & Therapy, 13(7), 527–533. https://doi.org/10.4161/cbt.19602

    Article  CAS  Google Scholar 

  99. Valdivia, A., Mingo, G., Aldana, V., Pinto, M. P., Ramirez, M., Retamal, C., et al. (2019). Fact or fiction, it is time for a verdict on vasculogenic mimicry? Frontiers in Oncology, 9, 680. https://doi.org/10.3389/fonc.2019.00680

    Article  PubMed  PubMed Central  Google Scholar 

  100. Zhang, X., Zhang, J., Zhou, H., Fan, G., & Li, Q. (2019). Molecular mechanisms and anticancer therapeutic strategies in vasculogenic mimicry. Journal of Cancer, 10(25), 6327–6340. https://doi.org/10.7150/jca.34171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Sun, T., Zhao, N., Zhao, X. L., Gu, Q., Zhang, S. W., Che, N., et al. (2010). Expression and functional significance of Twist1 in hepatocellular carcinoma: Its role in vasculogenic mimicry. Hepatology, 51(2), 545–556. https://doi.org/10.1002/hep.23311

    Article  CAS  PubMed  Google Scholar 

  102. Gong, W., Sun, B., Zhao, X., Zhang, D., Sun, J., Liu, T., et al. (2016). Nodal signaling promotes vasculogenic mimicry formation in breast cancer via the Smad2/3 pathway. Oncotarget, 7(43), 70152–70167. https://doi.org/10.18632/oncotarget.12161

    Article  PubMed  PubMed Central  Google Scholar 

  103. Bao, S., Jin, S., Wang, C., Tu, P., Hu, K., & Lu, J. (2020). Androgen receptor suppresses vasculogenic mimicry in hepatocellular carcinoma via circRNA7/miRNA7-5p/VE-cadherin/Notch4 signalling. Journal of Cellular and Molecular Medicine, 24(23), 14110–14120. https://doi.org/10.1111/jcmm.16022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Zan, S. J., Zhao, Y., Fang, T., & Chen, K. (2019). Expression of circular RNA hsa_circ_0014130 in lung adenocarcinoma cell lines and its effect on proliferation and invasion of lung adenocarcinoma cell line. Zhonghua Bing Li Xue Za Zhi, 48(12), 934–939. https://doi.org/10.3760/cma.j.issn.0529-5807.2019.12.004

    Article  CAS  PubMed  Google Scholar 

  105. Zhou, P., Xie, W., Huang, H. L., Huang, R. Q., Tian, C., Zhu, H. B., et al. (2020). circRNA_100859 functions as an oncogene in colon cancer by sponging the miR-217-HIF-1α pathway. Aging (Albany NY), 12(13), 13338–13353. https://doi.org/10.18632/aging.103438

    Article  CAS  Google Scholar 

  106. Zhai, Z., Fu, Q., Liu, C., Zhang, X., Jia, P., Xia, P., et al. (2019). Emerging roles of hsa-circ-0046600 targeting the miR-640/HIF-1α signalling pathway in the progression of HCC. Oncotargets and Therapy, 12, 9291–9302. https://doi.org/10.2147/ott.s229514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Qian, W., Huang, T., & Feng, W. (2020). Circular RNA HIPK3 promotes EMT of cervical cancer through sponging miR-338-3p to up-regulate HIF-1α. Cancer Management and Research, 12, 177–187. https://doi.org/10.2147/cmar.s232235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Shangguan, H., Feng, H., Lv, D., Wang, J., Tian, T., & Wang, X. (2020). Circular RNA circSLC25A16 contributes to the glycolysis of non-small-cell lung cancer through epigenetic modification. Cell Death & Disease, 11(6), 437. https://doi.org/10.1038/s41419-020-2635-5

    Article  CAS  Google Scholar 

  109. Xu, G., Li, M., Wu, J., Qin, C., Tao, Y., & He, H. (2020). Circular RNA circNRIP1 sponges microRNA-138-5p to maintain hypoxia-induced resistance to 5-fluorouracil through hif-1α-dependent glucose metabolism in gastric carcinoma. Cancer Management and Research, 12, 2789–2802. https://doi.org/10.2147/cmar.s246272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Peng, G., Meng, H., Pan, H., & Wang, W. (2021). CircRNA 001418 promoted cell growth and metastasis of bladder carcinoma via EphA2 by miR-1297. Current Molecular Pharmacology, 14(1), 68–78. https://doi.org/10.2174/1874467213666200505093815

    Article  CAS  PubMed  Google Scholar 

  111. Liu, L., Yang, X., Li, N. F., Lin, L., & Luo, H. (2019). Circ_0015756 promotes proliferation, invasion and migration by microRNA-7-dependent inhibition of FAK in hepatocellular carcinoma. Cell Cycle, 18(21), 2939–2953. https://doi.org/10.1080/15384101.2019.1664223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Wu, D., Xia, A., Fan, T., & Li, G. (2021). circRASGRF2 functions as an oncogenic gene in hepatocellular carcinoma by acting as a miR-1224 sponge. Molecular Therapy - Nucleic Acids, 23, 13–26. https://doi.org/10.1016/j.omtn.2020.10.035

    Article  CAS  PubMed  Google Scholar 

  113. Guan, X., Zong, Z. H., Liu, Y., Chen, S., Wang, L. L., & Zhao, Y. (2019). circPUM1 promotes tumorigenesis and progression of ovarian cancer by sponging miR-615-5p and miR-6753-5p. Molecular Therapy - Nucleic Acids, 18, 882–892. https://doi.org/10.1016/j.omtn.2019.09.032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. He, J. H., Han, Z. P., Luo, J. G., Jiang, J. W., Zhou, J. B., Chen, W. M., et al. (2020). Hsa_Circ_0007843 Acts as a mIR-518c-5p sponge to regulate the migration and invasion of colon cancer SW480 Cells. Frontiers in Genetics, 11, 9. https://doi.org/10.3389/fgene.2020.00009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Liu, H., Hu, G., Wang, Z., Liu, Q., Zhang, J., Chen, Y., et al. (2020). circPTCH1 promotes invasion and metastasis in renal cell carcinoma via regulating miR-485-5p/MMP14 axis. Theranostics, 10(23), 10791–10807. https://doi.org/10.7150/thno.47239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Xiao, H., & Liu, M. (2020). Circular RNA hsa_circ_0053277 promotes the development of colorectal cancer by upregulating matrix metallopeptidase 14 via miR-2467-3p sequestration. Journal of Cellular Physiology, 235(3), 2881–2890. https://doi.org/10.1002/jcp.29193

    Article  CAS  PubMed  Google Scholar 

  117. Delgado-Bellido, D., Serrano-Saenz, S., Fernández-Cortés, M., & Oliver, F. J. (2017). Vasculogenic mimicry signaling revisited: Focus on non-vascular VE-cadherin. Molecular Cancer, 16(1), 65. https://doi.org/10.1186/s12943-017-0631-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Seftor, E. A., Meltzer, P. S., Schatteman, G. C., Gruman, L. M., Hess, A. R., Kirschmann, D. A., et al. (2002). Expression of multiple molecular phenotypes by aggressive melanoma tumor cells: Role in vasculogenic mimicry. Critical Reviews in Oncology Hematology, 44(1), 17–27. https://doi.org/10.1016/s1040-8428(01)00199-8

    Article  PubMed  Google Scholar 

  119. Bartolomé, R. A., Torres, S., Isern de Val, S., Escudero-Paniagua, B., Calviño, E., Teixidó, J., et al. (2017). VE-cadherin RGD motifs promote metastasis and constitute a potential therapeutic target in melanoma and breast cancers. Oncotarget, 8(1), 215–227. https://doi.org/10.18632/oncotarget.13832

    Article  PubMed  Google Scholar 

  120. Hendrix, M. J., Seftor, E. A., Hess, A. R., & Seftor, R. E. (2003). Vasculogenic mimicry and tumour-cell plasticity: Lessons from melanoma. Nature Reviews Cancer, 3(6), 411–421. https://doi.org/10.1038/nrc1092

    Article  CAS  PubMed  Google Scholar 

  121. Yang, J., Zhu, D. M., Zhou, X. G., Yin, N., Zhang, Y., Zhang, Z. X., et al. (2017). HIF-2α promotes the formation of vasculogenic mimicry in pancreatic cancer by regulating the binding of Twist1 to the VE-cadherin promoter. Oncotarget, 8(29), 47801–47815. https://doi.org/10.18632/oncotarget.17999

    Article  PubMed  PubMed Central  Google Scholar 

  122. McAllister, J. C., Zhan, Q., Weishaupt, C., Hsu, M. Y., & Murphy, G. F. (2010). The embryonic morphogen, Nodal, is associated with channel-like structures in human malignant melanoma xenografts. Journal of Cutaneous Pathology, 37 Suppl 1(Suppl 1), 19–25. https://doi.org/10.1111/j.1600-0560.2010.01503.x

    Article  PubMed  Google Scholar 

  123. Topczewska, J. M., Postovit, L. M., Margaryan, N. V., Sam, A., Hess, A. R., Wheaton, W. W., et al. (2006). Embryonic and tumorigenic pathways converge via Nodal signaling: Role in melanoma aggressiveness. Nature Medicine, 12(8), 925–932. https://doi.org/10.1038/nm1448

    Article  CAS  PubMed  Google Scholar 

  124. Han, H., Du, L., Cao, Z., Zhang, B., & Zhou, Q. (2018). Triptonide potently suppresses pancreatic cancer cell-mediated vasculogenic mimicry by inhibiting expression of VE-cadherin and chemokine ligand 2 genes. European Journal of Pharmacology, 818, 593–603. https://doi.org/10.1016/j.ejphar.2017.11.019

    Article  CAS  PubMed  Google Scholar 

  125. Cao, W., Xu, C., Li, X., & Yang, X. (2019). Twist1 promotes astrocytoma development by stimulating vasculogenic mimicry. Oncology Letters, 18(1), 846–855. https://doi.org/10.3892/ol.2019.10380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Mao, X. G., Xue, X. Y., Wang, L., Zhang, X., Yan, M., Tu, Y. Y., et al. (2013). CDH5 is specifically activated in glioblastoma stemlike cells and contributes to vasculogenic mimicry induced by hypoxia. Neuro-Oncology, 15(7), 865–879. https://doi.org/10.1093/neuonc/not029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Hess, A. R., Seftor, E. A., Gruman, L. M., Kinch, M. S., Seftor, R. E., & Hendrix, M. J. (2006). VE-cadherin regulates EphA2 in aggressive melanoma cells through a novel signaling pathway: Implications for vasculogenic mimicry. Cancer Biology & Therapy, 5(2), 228–233. https://doi.org/10.4161/cbt.5.2.2510

    Article  CAS  Google Scholar 

  128. Paulis, Y. W., Soetekouw, P. M., Verheul, H. M., Tjan-Heijnen, V. C., & Griffioen, A. W. (2010). Signalling pathways in vasculogenic mimicry. Biochimica et Biophysica Acta, 1806(1), 18–28. https://doi.org/10.1016/j.bbcan.2010.01.001

    Article  CAS  PubMed  Google Scholar 

  129. Hendrix, M. J., Seftor, E. A., Meltzer, P. S., Gardner, L. M., Hess, A. R., Kirschmann, D. A., et al. (2001). Expression and functional significance of VE-cadherin in aggressive human melanoma cells: Role in vasculogenic mimicry. Proceedings of the National Academy of Sciences of the United States of America, 98(14), 8018–8023. https://doi.org/10.1073/pnas.131209798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Hess, A. R., Seftor, E. A., Gardner, L. M., Carles-Kinch, K., Schneider, G. B., Seftor, R. E., et al. (2001). Molecular regulation of tumor cell vasculogenic mimicry by tyrosine phosphorylation: Role of epithelial cell kinase (Eck/EphA2). Cancer Research, 61(8), 3250–3255.

    CAS  PubMed  Google Scholar 

  131. Margaryan, N. V., Strizzi, L., Abbott, D. E., Seftor, E. A., Rao, M. S., Hendrix, M. J., et al. (2009). EphA2 as a promoter of melanoma tumorigenicity. Cancer Biology & Therapy, 8(3), 279–288. https://doi.org/10.4161/cbt.8.3.7485

    Article  CAS  Google Scholar 

  132. Sulzmaier, F. J., Jean, C., & Schlaepfer, D. D. (2014). FAK in cancer: Mechanistic findings and clinical applications. Nature Reviews Cancer, 14(9), 598–610. https://doi.org/10.1038/nrc3792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Lu, X. S., Sun, W., Ge, C. Y., Zhang, W. Z., & Fan, Y. Z. (2013). Contribution of the PI3K/MMPs/Ln-5γ2 and EphA2/FAK/Paxillin signaling pathways to tumor growth and vasculogenic mimicry of gallbladder carcinomas. International Journal of Oncology, 42(6), 2103–2115. https://doi.org/10.3892/ijo.2013.1897

    Article  CAS  PubMed  Google Scholar 

  134. Zhang, J. T., Sun, W., Zhang, W. Z., Ge, C. Y., Liu, Z. Y., Zhao, Z. M., et al. (2014). Norcantharidin inhibits tumor growth and vasculogenic mimicry of human gallbladder carcinomas by suppression of the PI3-K/MMPs/Ln-5γ2 signaling pathway. BMC Cancer, 14, 193. https://doi.org/10.1186/1471-2407-14-193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Duxbury, M. S., Ito, H., Zinner, M. J., Ashley, S. W., & Whang, E. E. (2004). Ligation of EphA2 by Ephrin A1-Fc inhibits pancreatic adenocarcinoma cellular invasiveness. Biochemical and Biophysical Research Communications, 320(4), 1096–1102. https://doi.org/10.1016/j.bbrc.2004.06.054

    Article  CAS  PubMed  Google Scholar 

  136. Hess, A. R., & Hendrix, M. J. (2006). Focal adhesion kinase signaling and the aggressive melanoma phenotype. Cell Cycle, 5(5), 478–480. https://doi.org/10.4161/cc.5.5.2518

    Article  CAS  PubMed  Google Scholar 

  137. Fernandez-Cortes, M., Delgado-Bellido, D., & Oliver, F. J. (2019). Vasculogenic mimicry: Become an endothelial cell “but not so much.” Frontiers in Oncology, 9, 803. https://doi.org/10.3389/fonc.2019.00803

    Article  PubMed  PubMed Central  Google Scholar 

  138. Delgado-Bellido, D., Fernández-Cortés, M., Rodríguez, M. I., Serrano-Sáenz, S., Carracedo, A., Garcia-Diaz, A., et al. (2019). VE-cadherin promotes vasculogenic mimicry by modulating kaiso-dependent gene expression. Cell Death and Differentiation, 26(2), 348–361. https://doi.org/10.1038/s41418-018-0125-4

    Article  CAS  PubMed  Google Scholar 

  139. Lissitzky, J. C., Parriaux, D., Ristorcelli, E., Vérine, A., Lombardo, D., & Verrando, P. (2009). Cyclic AMP signaling as a mediator of vasculogenic mimicry in aggressive human melanoma cells in vitro. Cancer Research, 69(3), 802–809. https://doi.org/10.1158/0008-5472.can-08-2391

    Article  CAS  PubMed  Google Scholar 

  140. Yousif, L. F., Di Russo, J., & Sorokin, L. (2013). Laminin isoforms in endothelial and perivascular basement membranes. Cell Adhesion & Migration, 7(1), 101–110. https://doi.org/10.4161/cam.22680

    Article  Google Scholar 

  141. Seftor, R. E., Seftor, E. A., Koshikawa, N., Meltzer, P. S., Gardner, L. M., Bilban, M., et al. (2001). 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 Research, 61(17), 6322–6327.

    CAS  PubMed  Google Scholar 

  142. Hess, A. R., Seftor, E. A., Seftor, R. E., & Hendrix, M. J. (2003). Phosphoinositide 3-kinase regulates membrane Type 1-matrix metalloproteinase (MMP) and MMP-2 activity during melanoma cell vasculogenic mimicry. Cancer Research, 63(16), 4757–4762.

    CAS  PubMed  Google Scholar 

  143. Sood, A. K., Fletcher, M. S., Coffin, J. E., Yang, M., Seftor, E. A., Gruman, L. M., et al. (2004). Functional role of matrix metalloproteinases in ovarian tumor cell plasticity. American Journal of Obstetrics and Gynecology, 190(4), 899–909. https://doi.org/10.1016/j.ajog.2004.02.011

    Article  CAS  PubMed  Google Scholar 

  144. Winkler, F. (2017). Hostile takeover: How tumours hijack pre-existing vascular environments to thrive. The Journal of Pathology, 242(3), 267–272. https://doi.org/10.1002/path.4904

    Article  PubMed  Google Scholar 

  145. Hirschi, K. K., Rohovsky, S. A., & D’Amore, P. A. (1998). PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. Journal of Cell Biology, 141(3), 805–814. https://doi.org/10.1083/jcb.141.3.805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Yang, Z., Yao, H., Fei, F., Li, Y., Qu, J., Li, C., et al. (2018). Generation of erythroid cells from polyploid giant cancer cells: Re-thinking about tumor blood supply. Journal of Cancer Research and Clinical Oncology, 144(4), 617–627. https://doi.org/10.1007/s00432-018-2598-4

    Article  PubMed  Google Scholar 

  147. Liu, Q., Qiao, L., Liang, N., Xie, J., Zhang, J., Deng, G., et al. (2016). The relationship between vasculogenic mimicry and epithelial-mesenchymal transitions. Journal of Cellular and Molecular Medicine, 20(9), 1761–1769. https://doi.org/10.1111/jcmm.12851

    Article  PubMed  PubMed Central  Google Scholar 

  148. Wagenblast, E., Soto, M., Gutiérrez-Ángel, S., Hartl, C. A., Gable, A. L., Maceli, A. R., et al. (2015). A model of breast cancer heterogeneity reveals vascular mimicry as a driver of metastasis. Nature, 520(7547), 358–362. https://doi.org/10.1038/nature14403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Lai, C. Y., Schwartz, B. E., & Hsu, M. Y. (2012). CD133+ melanoma subpopulations contribute to perivascular niche morphogenesis and tumorigenicity through vasculogenic mimicry. Cancer Research, 72(19), 5111–5118. https://doi.org/10.1158/0008-5472.can-12-0624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Zhao, H., Chen, S., & Fu, Q. (2020). Exosomes from CD133(+) cells carrying circ-ABCC1 mediate cell stemness and metastasis in colorectal cancer. Journal of Cellular Biochemistry, 121(5–6), 3286–3297. https://doi.org/10.1002/jcb.29600

    Article  CAS  PubMed  Google Scholar 

  151. Chen, L., Zhou, H., & Guan, Z. (2019). CircRNA_000543 knockdown sensitizes nasopharyngeal carcinoma to irradiation by targeting miR-9/platelet-derived growth factor receptor B axis. Biochemical and Biophysical Research Communications, 512(4), 786–792. https://doi.org/10.1016/j.bbrc.2019.03.126

    Article  CAS  PubMed  Google Scholar 

  152. Xiang, T., Lin, Y. X., Ma, W., Zhang, H. J., Chen, K. M., He, G. P., et al. (2018). Vasculogenic mimicry formation in EBV-associated epithelial malignancies. Nature Communications, 9(1), 5009. https://doi.org/10.1038/s41467-018-07308-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Xu, S., Bai, J., Zhuan, Z., Li, B., Zhang, Z., Wu, X., et al. (2018). EBV-LMP1 is involved in vasculogenic mimicry formation via VEGFA/VEGFR1 signaling in nasopharyngeal carcinoma. Oncology Reports, 40(1), 377–384. https://doi.org/10.3892/or.2018.6414

    Article  CAS  PubMed  Google Scholar 

  154. David, J. M., Dominguez, C., Hamilton, D. H., & Palena, C. (2016). The IL-8/IL-8R Axis: A Double Agent in Tumor Immune Resistance. Vaccines (Basel), 4(3), https://doi.org/10.3390/vaccines4030022

  155. Dwyer, J., Hebda, J. K., Le Guelte, A., Galan-Moya, E. M., Smith, S. S., Azzi, S., et al. (2012). Glioblastoma cell-secreted interleukin-8 induces brain endothelial cell permeability via CXCR2. PLoS ONE, 7(9), e45562. https://doi.org/10.1371/journal.pone.0045562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Logue, S. E., McGrath, E. P., Cleary, P., Greene, S., Mnich, K., Almanza, A., et al. (2018). Inhibition of IRE1 RNase activity modulates the tumor cell secretome and enhances response to chemotherapy. Nature Communications, 9(1), 3267. https://doi.org/10.1038/s41467-018-05763-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Mutalifu, N., Du, P., Zhang, J., Akbar, H., Yan, B., Alimu, S., et al. (2020). Circ_0000215 Increases the expression of CXCR2 and promoted the progression of glioma cells by sponging miR-495-3p. Technology in Cancer Research & Treatment, 19, 1533033820957026. https://doi.org/10.1177/1533033820957026

    Article  CAS  Google Scholar 

  158. Seaman, S., Zhu, Z., Saha, S., Zhang, X. M., Yang, M. Y., Hilton, M. B., et al. (2017). Eradication of tumors through simultaneous ablation of CD276/B7-H3-positive tumor cells and tumor vasculature. Cancer Cell, 31(4), 501-515.e508. https://doi.org/10.1016/j.ccell.2017.03.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Wang, L., Zhang, G. C., Kang, F. B., Zhang, L., & Zhang, Y. Z. (2019). hsa_circ0021347 as a potential target regulated by B7–H3 in modulating the malignant characteristics of osteosarcoma. BioMed Research International, 2019, 9301989. https://doi.org/10.1155/2019/9301989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Zeng, Y., Yao, X., Liu, X., He, X., Li, L., Liu, X., et al. (2019). Anti-angiogenesis triggers exosomes release from endothelial cells to promote tumor vasculogenesis. The Journal of Extracellular Vesicles, 8(1), 1629865. https://doi.org/10.1080/20013078.2019.1629865

    Article  CAS  PubMed  Google Scholar 

  161. Huang, X. Y., Huang, Z. L., Huang, J., Xu, B., Huang, X. Y., Xu, Y. H., et al. (2020). Exosomal circRNA-100338 promotes hepatocellular carcinoma metastasis via enhancing invasiveness and angiogenesis. Journal of Experimental & Clinical Cancer Research, 39(1), 20. https://doi.org/10.1186/s13046-020-1529-9

    Article  CAS  Google Scholar 

  162. Rezaei, M., Martins Cavaco, A. C., Stehling, M., Nottebaum, A., Brockhaus, K., Caliandro, M. F., et al. (2020). Extracellular vesicle transfer from endothelial cells drives VE-cadherin expression in breast cancer cells, thereby causing heterotypic cell contacts. Cancers (Basel), 12(8), https://doi.org/10.3390/cancers12082138

  163. Bergers, G., & Fendt, S. M. (2021). The metabolism of cancer cells during metastasis. Nature Reviews Cancer, 21(3), 162–180. https://doi.org/10.1038/s41568-020-00320-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Zhang, H., & Lu, B. (2020). The roles of ceRNAs-mediated autophagy in cancer chemoresistance and metastasis. Cancers (Basel), 12(10), https://doi.org/10.3390/cancers12102926

  165. Zang, J., Lu, D., & Xu, A. (2020). The interaction of circRNAs and RNA binding proteins: An important part of circRNA maintenance and function. Journal of Neuroscience Research, 98(1), 87–97. https://doi.org/10.1002/jnr.24356

    Article  CAS  PubMed  Google Scholar 

  166. Shang, Q., Yang, Z., Jia, R., & Ge, S. (2019). The novel roles of circRNAs in human cancer. Molecular Cancer, 18(1), 6. https://doi.org/10.1186/s12943-018-0934-6

    Article  PubMed  PubMed Central  Google Scholar 

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This manuscript is supported by a grant from the National Natural Scientific Foundations of China (81872112).

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Shao, Y., Lu, B. The emerging roles of circular RNAs in vessel co-option and vasculogenic mimicry: clinical insights for anti-angiogenic therapy in cancers. Cancer Metastasis Rev 41, 173–191 (2022). https://doi.org/10.1007/s10555-021-10000-8

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