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Angiotropism, Pericytic Mimicry and Extravascular Migratory Metastasis in Melanoma: An Alternative to Intravascular Cancer Dissemination

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Cancer Microenvironment

Abstract

For more than 15 years, angiotropism in melanoma has been emphasized as a marker of extravascular migration of tumor cells along the abluminal vascular surface, unveiling an alternative mechanism of tumor spread distinct from intravascular dissemination. This mechanism has been termed extravascular migratory metastasis (EVMM). During EVMM, angiotropic tumor cells migrate in a ‘pericytic-like’ manner (pericytic mimicry) along the external surfaces of vascular channels, without intravasation. Through this pathway, melanoma cells may spread to nearby or more distant sites. Angiotropism is a prognostic factor predicting risk for metastasis in human melanoma, and a marker of EVMM in several experimental models. Importantly, analogies of EVMM and pericytic mimicry include neural crest cell migration, vasculogenesis and angiogenesis, and recent studies have suggested that the interaction between melanoma cells and the abluminal vascular surface induce differential expression of genes reminiscent of cancer migration and embryonic/stem cell state transitions. A recent work revealed that repetitive UV exposure of primary cutaneous melanomas in a genetically engineered mouse model promotes metastatic progression via angiotropism and migration along the abluminal vascular surface. Finally, recent data using imaging of melanoma cells in a murine model have shown the progression of tumor cells along the vascular surfaces. Taken together, these data provide support for the biological phenomenon of angiotropism and EVMM, which may open promising new strategies for reducing or preventing melanoma metastasis.

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Acknowledgments

In vivo confocal imaging shown in Fig. 5 was performed at the California NanoSystems Institute (CNSI) Advanced Light Microscopy/Spectroscopy Shared Resource Facility at UCLA with support from a NIH/National Center for Advancing Translational Science UCLA CTSI Grant (UL1TR000124).

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Authors and Affiliations

  1. Department of Pathology and Laboratory Medicine and Jonsson Comprehensive Cancer Center, David Geffen School of Medicine at University of California Los Angeles UCLA, Los Angeles, CA, USA

    Claire Lugassy, Madhuri Wadehra & Raymond L. Barnhill

  2. Department of Neurology, University of California San Francisco UCSF, San Francisco, CA, USA

    Sohila Zadran

  3. California Institute of Quantitative Biosciences, San Francisco, CA, USA

    Sohila Zadran

  4. Advanced Light Microscopy/Spectroscopy Lab, California NanoSystems Institute and Department ofChemistry and Biochemistry, University of California Los Angeles (UCLA), Los Angeles, CA, USA

    Laurent A. Bentolila

  5. Department of Neurology, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA

    Roshini Prakash & S. Thomas Carmichael

  6. National Institutes of Health, Bethesda, MD, USA

    Hynda K. Kleinman

  7. Orthopedic Hospital Research Center and Broad Stem Cell Center, David Geffen School of Medicine at University of California Los Angeles, Los Angeles, CA, USA

    Bruno Péault

  8. MRC Center for Regenerative Medicine and BHF Center for Cardiovascular Science, Queens Medical Research Institute University of Edinburgh, Edinburgh, UK

    Bruno Péault

  9. Institut Curie, Normal and Pathological Development of Melanocytes, Orsay, France

    Lionel Larue

  10. CNRS UMR3347, Orsay, France

    Lionel Larue

  11. INSERM U1021, Orsay, France

    Lionel Larue

  12. Department of Pathology, Institut Curie, Los Paris, France

    Raymond L. Barnhill

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  1. Claire Lugassy
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  2. Sohila Zadran
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Correspondence to Claire Lugassy.

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Lugassy, C., Zadran, S., Bentolila, L.A. et al. Angiotropism, Pericytic Mimicry and Extravascular Migratory Metastasis in Melanoma: An Alternative to Intravascular Cancer Dissemination. Cancer Microenvironment 7, 139–152 (2014). https://doi.org/10.1007/s12307-014-0156-4

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