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Vessel co-option and angiotropic extravascular migratory metastasis: a continuum of tumour growth and spread?

British Journal of Cancer volume 126, pages 973–980 (2022)Cite this article

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Abstract

Two fields of cancer research have emerged dealing with the biology of tumour cells localised to the abluminal vascular surface: vessel co-option (VCo), a non-angiogenic mode of tumour growth and angiotropic extravascular migratory metastasis (EVMM), a non-hematogenous mode of tumour migration and metastasis. VCo is a mechanism by which tumour cells gain access to a blood supply by spreading along existing blood vessels in order to grow locally. Angiotropic EVMM involves “pericytic mimicry” (PM), which is characterised by tumour cells continuously migrating in the place of pericytes distantly along abluminal vascular surfaces. When cancer cells are engaged in PM and EVMM, they migrate along blood vessels beyond the advancing front of the tumour to secondary sites with the formation of regional and distant metastases. In the present perspective, the authors review the current scientific literature, emphasising the analogies between embryogenesis and cancer progression, the re-activation of embryonic signals by “cancer stem cells”, and the important role of laminins and epithelial-mesenchymal-transition. This perspective maintains that VCo and angiotropic EVMM constitute complementary processes and represent a continuum of cancer progression from the primary tumour to metastases and of tumour growth to EVMM, analogous to the embryonic development program.

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Fig. 1: Recapitulation of tumour progression via a continuum of vessel co-option (VCo)/growth and angiotropic extravascular migratory metastasis (EVMM) illustrated by images from cutaneous and ocular melanoma progression.
Fig. 2: Replacement HPG demonstrating PM/VCo in liver metastases originating from different types of primary tumours.

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Acknowledgements

We sincerely thank Maud Haon who designed the diagram for Fig. 1.

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Authors and Affiliations

  1. Department of Translational Research, Institut Curie, Paris, France

    Claire Lugassy & Raymond L. Barnhill

  2. Translational Cancer Research Unit, GZA Hospitals, Sint-Augustinus, Antwerp, Belgium

    Peter B. Vermeulen

  3. Center for Oncological Research (CORE, Faculty of Medicine and Health Sciences), University of Antwerp, Wilrijk, Antwerp, Belgium

    Peter B. Vermeulen

  4. Department of Basic Medical Sciences, Neurosciences and Sensory Organs, University of Bari Medical School, Bari, Italy

    Domenico Ribatti

  5. Nuffield Division of Clinical Laboratory Sciences, Radcliffe Department of Medicine, University of Oxford, John Radcliffe Hospital, Oxford, UK

    Francesco Pezzella

  6. University of Paris UFR de Médecine, Paris, France

    Raymond L. Barnhill

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CL and RB designed and wrote the manuscript with essential inputs from DR, FP and PV. All authors reviewed the manuscript.

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Correspondence to Claire Lugassy.

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Lugassy, C., Vermeulen, P.B., Ribatti, D. et al. Vessel co-option and angiotropic extravascular migratory metastasis: a continuum of tumour growth and spread?. Br J Cancer 126, 973–980 (2022). https://doi.org/10.1038/s41416-021-01686-2

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