Control of MT1-MMP transport by atypical PKC during breast-cancer progression

Carine Rosse; Catalina Lodillinsky; Laetitia Fuhrmann; Maya Nourieh; Pedro Monteiro; Marie Irondelle; Emilie Lagoutte; Sophie Vacher; Francois Waharte; Perrine Paul-Gilloteaux; Maryse Romao; Lucie Sengmanivong; Mark Linch; Johan van Lint; Graca Raposo; Anne Vincent-Salomon; Ivan Bieche; Peter J. Parker; Philippe Chavrier

doi:10.1073/pnas.1400749111

Control of MT1-MMP transport by atypical PKC during breast-cancer progression

Carine Rosse^*, Catalina Lodillinsky, Laetitia Fuhrmann, Maya Nourieh, Pedro Monteiro, Marie Irondelle, Emilie Lagoutte, Sophie Vacher, Francois Waharte, Perrine Paul-Gilloteaux, Maryse Romao, Lucie Sengmanivong, Mark Linch, Johan van Lint, Graca Raposo, Anne Vincent-Salomon, Ivan Bieche, Peter J. Parker, Philippe Chavrier

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

75 Citations (Scopus)

Abstract

Dissemination of carcinoma cells requires the pericellular degradation of the extracellular matrix, which is mediated by membrane type 1-matrix metalloproteinase (MT1-MMP). In this article, we report a co-up-regulation and colocalization of MT1-MMP and atypical protein kinase C iota (aPKC iota) in hormone receptor-negative breast tumors in association with a higher risk of metastasis. Silencing of aPKC in invasive breast-tumor cell lines impaired the delivery of MT1-MMP from late endocytic storage compartments to the surface and inhibited matrix degradation and invasion. We provide evidence that aPKC iota, in association with MT1-MMP-containing endosomes, phosphorylates cortactin, which is present in F-actin-rich puncta on MT1-MMP-positive endosomes and regulates cortactin association with the membrane scission protein dynamin-2. Thus, cell line-based observations and clinical data reveal the concerted activity of aPKC, cortactin, and dynamin-2, which control the trafficking of MT1-MMP from late endosome to the plasma membrane and play an important role in the invasive potential of breast-cancer cells.

Original language	English
Pages (from-to)	E1872-E1879
Number of pages	8
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	111
Issue number	18
DOIs	https://doi.org/10.1073/pnas.1400749111
Publication status	Published - 6 May 2014

Keywords

membrane traffic
actin cytoskeleton
multi-vesicular body
MMP14
EXTRACELLULAR-MATRIX DEGRADATION
CELL INVASION
TUMOR-CELLS
INVADOPODIA FORMATION
CORTACTIN
METALLOPROTEINASE
EXPRESSION
POLARITY
OVEREXPRESSION
METASTASIS

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1073/pnas.1400749111

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Rosse, C., Lodillinsky, C., Fuhrmann, L., Nourieh, M., Monteiro, P., Irondelle, M., Lagoutte, E., Vacher, S., Waharte, F., Paul-Gilloteaux, P., Romao, M., Sengmanivong, L., Linch, M., van Lint, J., Raposo, G., Vincent-Salomon, A., Bieche, I., Parker, P. J., & Chavrier, P. (2014). Control of MT1-MMP transport by atypical PKC during breast-cancer progression. Proceedings of the National Academy of Sciences of the United States of America, 111(18), E1872-E1879. https://doi.org/10.1073/pnas.1400749111

@article{a7f49362e4c04299ae4fd6665667782b,

title = "Control of MT1-MMP transport by atypical PKC during breast-cancer progression",

abstract = "Dissemination of carcinoma cells requires the pericellular degradation of the extracellular matrix, which is mediated by membrane type 1-matrix metalloproteinase (MT1-MMP). In this article, we report a co-up-regulation and colocalization of MT1-MMP and atypical protein kinase C iota (aPKC iota) in hormone receptor-negative breast tumors in association with a higher risk of metastasis. Silencing of aPKC in invasive breast-tumor cell lines impaired the delivery of MT1-MMP from late endocytic storage compartments to the surface and inhibited matrix degradation and invasion. We provide evidence that aPKC iota, in association with MT1-MMP-containing endosomes, phosphorylates cortactin, which is present in F-actin-rich puncta on MT1-MMP-positive endosomes and regulates cortactin association with the membrane scission protein dynamin-2. Thus, cell line-based observations and clinical data reveal the concerted activity of aPKC, cortactin, and dynamin-2, which control the trafficking of MT1-MMP from late endosome to the plasma membrane and play an important role in the invasive potential of breast-cancer cells.",

keywords = "membrane traffic, actin cytoskeleton, multi-vesicular body, MMP14, EXTRACELLULAR-MATRIX DEGRADATION, CELL INVASION, TUMOR-CELLS, INVADOPODIA FORMATION, CORTACTIN, METALLOPROTEINASE, EXPRESSION, POLARITY, OVEREXPRESSION, METASTASIS",

author = "Carine Rosse and Catalina Lodillinsky and Laetitia Fuhrmann and Maya Nourieh and Pedro Monteiro and Marie Irondelle and Emilie Lagoutte and Sophie Vacher and Francois Waharte and Perrine Paul-Gilloteaux and Maryse Romao and Lucie Sengmanivong and Mark Linch and {van Lint}, Johan and Graca Raposo and Anne Vincent-Salomon and Ivan Bieche and Parker, {Peter J.} and Philippe Chavrier",

year = "2014",

month = may,

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doi = "10.1073/pnas.1400749111",

language = "English",

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Rosse, C, Lodillinsky, C, Fuhrmann, L, Nourieh, M, Monteiro, P, Irondelle, M, Lagoutte, E, Vacher, S, Waharte, F, Paul-Gilloteaux, P, Romao, M, Sengmanivong, L, Linch, M, van Lint, J, Raposo, G, Vincent-Salomon, A, Bieche, I, Parker, PJ & Chavrier, P 2014, 'Control of MT1-MMP transport by atypical PKC during breast-cancer progression', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 18, pp. E1872-E1879. https://doi.org/10.1073/pnas.1400749111

TY - JOUR

T1 - Control of MT1-MMP transport by atypical PKC during breast-cancer progression

AU - Rosse, Carine

AU - Lodillinsky, Catalina

AU - Fuhrmann, Laetitia

AU - Nourieh, Maya

AU - Monteiro, Pedro

AU - Irondelle, Marie

AU - Lagoutte, Emilie

AU - Vacher, Sophie

AU - Waharte, Francois

AU - Paul-Gilloteaux, Perrine

AU - Romao, Maryse

AU - Sengmanivong, Lucie

AU - Linch, Mark

AU - van Lint, Johan

AU - Raposo, Graca

AU - Vincent-Salomon, Anne

AU - Bieche, Ivan

AU - Parker, Peter J.

AU - Chavrier, Philippe

PY - 2014/5/6

Y1 - 2014/5/6

N2 - Dissemination of carcinoma cells requires the pericellular degradation of the extracellular matrix, which is mediated by membrane type 1-matrix metalloproteinase (MT1-MMP). In this article, we report a co-up-regulation and colocalization of MT1-MMP and atypical protein kinase C iota (aPKC iota) in hormone receptor-negative breast tumors in association with a higher risk of metastasis. Silencing of aPKC in invasive breast-tumor cell lines impaired the delivery of MT1-MMP from late endocytic storage compartments to the surface and inhibited matrix degradation and invasion. We provide evidence that aPKC iota, in association with MT1-MMP-containing endosomes, phosphorylates cortactin, which is present in F-actin-rich puncta on MT1-MMP-positive endosomes and regulates cortactin association with the membrane scission protein dynamin-2. Thus, cell line-based observations and clinical data reveal the concerted activity of aPKC, cortactin, and dynamin-2, which control the trafficking of MT1-MMP from late endosome to the plasma membrane and play an important role in the invasive potential of breast-cancer cells.

AB - Dissemination of carcinoma cells requires the pericellular degradation of the extracellular matrix, which is mediated by membrane type 1-matrix metalloproteinase (MT1-MMP). In this article, we report a co-up-regulation and colocalization of MT1-MMP and atypical protein kinase C iota (aPKC iota) in hormone receptor-negative breast tumors in association with a higher risk of metastasis. Silencing of aPKC in invasive breast-tumor cell lines impaired the delivery of MT1-MMP from late endocytic storage compartments to the surface and inhibited matrix degradation and invasion. We provide evidence that aPKC iota, in association with MT1-MMP-containing endosomes, phosphorylates cortactin, which is present in F-actin-rich puncta on MT1-MMP-positive endosomes and regulates cortactin association with the membrane scission protein dynamin-2. Thus, cell line-based observations and clinical data reveal the concerted activity of aPKC, cortactin, and dynamin-2, which control the trafficking of MT1-MMP from late endosome to the plasma membrane and play an important role in the invasive potential of breast-cancer cells.

KW - membrane traffic

KW - actin cytoskeleton

KW - multi-vesicular body

KW - MMP14

KW - EXTRACELLULAR-MATRIX DEGRADATION

KW - CELL INVASION

KW - TUMOR-CELLS

KW - INVADOPODIA FORMATION

KW - CORTACTIN

KW - METALLOPROTEINASE

KW - EXPRESSION

KW - POLARITY

KW - OVEREXPRESSION

KW - METASTASIS

U2 - 10.1073/pnas.1400749111

DO - 10.1073/pnas.1400749111

M3 - Article

SN - 0027-8424

VL - 111

SP - E1872-E1879

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 18

ER -

Control of MT1-MMP transport by atypical PKC during breast-cancer progression

Abstract

Keywords

UN SDGs

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