Diverse matrix metalloproteinase functions regulate cancer amoeboid migration

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, Sophia N. Karagiannis and Victoria Sanz-Moreno ()
Additional contact information
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

Nature Communications, 2014, vol. 5, issue 1, 1-13

Abstract: 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.

Date: 2014
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DOI: 10.1038/ncomms5255

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