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Diverse matrix metalloproteinase functions regulate cancer amoeboid migration

Author

Listed:
  • Jose L. Orgaz

    (Tumour Plasticity Team, King’s College London, New Hunt’s House, Guy’s Campus)

  • Pahini Pandya

    (Tumour Plasticity Team, King’s College London, New Hunt’s House, Guy’s Campus)

  • Rimple Dalmeida

    (Tumour Plasticity Team, King’s College London, New Hunt’s House, Guy’s Campus)

  • Panagiotis Karagiannis

    (NIHR Biomedical Research Centre at Guy’s and St Thomas’ Hospitals, Cutaneous Medicine and Immunotherapy Unit, St John’s Institute of Dermatology, King’s College London)

  • Berta Sanchez-Laorden

    (Molecular Oncology Group, Cancer Research UK Manchester Institute, The University of Manchester)

  • Amaya Viros

    (Molecular Oncology Group, Cancer Research UK Manchester Institute, The University of Manchester)

  • Jean Albrengues

    (INSERM, U1081, CNRS, UMR7284, Institute for Research on Cancer and Aging in Nice (IRCAN), Faculté de Médecine, University of Nice Sophia-Antipolis)

  • Frank O. Nestle

    (NIHR Biomedical Research Centre at Guy’s and St Thomas’ Hospitals, Cutaneous Medicine and Immunotherapy Unit, St John’s Institute of Dermatology, King’s College London)

  • Anne J. Ridley

    (Cell Signalling in Invasion and Motility Team, King’s College London, New Hunt’s House, Guy’s Campus)

  • Cedric Gaggioli

    (INSERM, U1081, CNRS, UMR7284, Institute for Research on Cancer and Aging in Nice (IRCAN), Faculté de Médecine, University of Nice Sophia-Antipolis)

  • Richard Marais

    (Molecular Oncology Group, Cancer Research UK Manchester Institute, The University of Manchester)

  • Sophia N. Karagiannis

    (NIHR Biomedical Research Centre at Guy’s and St Thomas’ Hospitals, Cutaneous Medicine and Immunotherapy Unit, St John’s Institute of Dermatology, King’s College London)

  • Victoria Sanz-Moreno

    (Tumour Plasticity Team, King’s College London, New Hunt’s House, Guy’s Campus)

Abstract

Rounded-amoeboid cancer cells use actomyosin contractility driven by Rho-ROCK and JAK-STAT3 to migrate efficiently. It has been suggested that rounded-amoeboid cancer cells do not require matrix metalloproteinases (MMPs) to invade. Here we compare MMP levels in rounded-amoeboid and elongated-mesenchymal melanoma cells. Surprisingly, we find that rounded-amoeboid melanoma cells secrete higher levels of several MMPs, including collagenase MMP-13 and gelatinase MMP-9. As a result, rounded-amoeboid melanoma cells degrade collagen I more efficiently than elongated-mesenchymal cells. Furthermore, using a non-catalytic mechanism, MMP-9 promotes rounded-amoeboid 3D migration through regulation of actomyosin contractility via CD44 receptor. MMP-9 is upregulated in a panel of rounded-amoeboid compared with elongated-mesenchymal melanoma cell lines and its levels are controlled by ROCK-JAK-STAT3 signalling. MMP-9 expression increases during melanoma progression and it is particularly prominent in the invasive fronts of lesions, correlating with cell roundness. Therefore, rounded-amoeboid cells use both catalytic and non-catalytic activities of MMPs for invasion.

Suggested Citation

  • Jose L. Orgaz & Pahini Pandya & Rimple Dalmeida & Panagiotis Karagiannis & Berta Sanchez-Laorden & Amaya Viros & Jean Albrengues & Frank O. Nestle & Anne J. Ridley & Cedric Gaggioli & Richard Marais &, 2014. "Diverse matrix metalloproteinase functions regulate cancer amoeboid migration," Nature Communications, Nature, vol. 5(1), pages 1-13, September.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms5255
    DOI: 10.1038/ncomms5255
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    Cited by:

    1. Shasha Yao & Yi Wang & Qian Tang & Yujie Yin & Yu Geng & Lei Xu & Shifu Liang & Jiajia Xiang & Jiaqi Fan & Jianbin Tang & Jian Liu & Shiqun Shao & Youqing Shen, 2024. "A plug-and-play monofunctional platform for targeted degradation of extracellular proteins and vesicles," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Eva Crosas-Molist & Vittoria Graziani & Oscar Maiques & Pahini Pandya & Joanne Monger & Remi Samain & Samantha L. George & Saba Malik & Jerrine Salise & Valle Morales & Adrien Le Guennec & R. Andrew A, 2023. "AMPK is a mechano-metabolic sensor linking cell adhesion and mitochondrial dynamics to Myosin-dependent cell migration," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

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