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Ultraviolet light-induced collagen degradation inhibits melanoma invasion

Author

Listed:
  • Timothy Budden

    (The University of Manchester)

  • Caroline Gaudy-Marqueste

    (Aix-Marseille University)

  • Andrew Porter

    (The University of Manchester, Alderley Park)

  • Emily Kay

    (University of Glasgow
    CRUK Beatson Institute)

  • Shilpa Gurung

    (The University of Manchester)

  • Charles H. Earnshaw

    (The University of Manchester)

  • Katharina Roeck

    (The University of Manchester)

  • Sarah Craig

    (The University of Manchester)

  • Víctor Traves

    (Institut Valencià Oncologia)

  • Jean Krutmann

    (IUF – Leibniz Research Institute of Environmental Medicine
    Heinrich-Heine-University)

  • Patricia Muller

    (The University of Manchester)

  • Luisa Motta

    (The University of Manchester)

  • Sara Zanivan

    (University of Glasgow
    CRUK Beatson Institute)

  • Angeliki Malliri

    (The University of Manchester, Alderley Park)

  • Simon J. Furney

    (Royal College of Surgeons in
    Royal College of Surgeons in Ireland Dublin)

  • Eduardo Nagore

    (Institut Valencià Oncologia)

  • Amaya Virós

    (The University of Manchester)

Abstract

Ultraviolet radiation (UVR) damages the dermis and fibroblasts; and increases melanoma incidence. Fibroblasts and their matrix contribute to cancer, so we studied how UVR modifies dermal fibroblast function, the extracellular matrix (ECM) and melanoma invasion. We confirmed UVR-damaged fibroblasts persistently upregulate collagen-cleaving matrix metalloprotein-1 (MMP1) expression, reducing local collagen (COL1A1), and COL1A1 degradation by MMP1 decreased melanoma invasion. Conversely, inhibiting ECM degradation and MMP1 expression restored melanoma invasion. Primary cutaneous melanomas of aged humans show more cancer cells invade as single cells at the invasive front of melanomas expressing and depositing more collagen, and collagen and single melanoma cell invasion are robust predictors of poor melanoma-specific survival. Thus, primary melanomas arising over collagen-degraded skin are less invasive, and reduced invasion improves survival. However, melanoma-associated fibroblasts can restore invasion by increasing collagen synthesis. Finally, high COL1A1 gene expression is a biomarker of poor outcome across a range of primary cancers.

Suggested Citation

  • Timothy Budden & Caroline Gaudy-Marqueste & Andrew Porter & Emily Kay & Shilpa Gurung & Charles H. Earnshaw & Katharina Roeck & Sarah Craig & Víctor Traves & Jean Krutmann & Patricia Muller & Luisa Mo, 2021. "Ultraviolet light-induced collagen degradation inhibits melanoma invasion," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-22953-z
    DOI: 10.1038/s41467-021-22953-z
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    Cited by:

    1. Alessio Magis & Michaela Limmer & Venkat Mudiyam & David Monchaud & Stefan Juranek & Katrin Paeschke, 2023. "UV-induced G4 DNA structures recruit ZRF1 which prevents UV-induced senescence," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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