The tumor cell-secreted matricellular protein WISP1 drives pro-metastatic collagen linearization.
Animals
Breast Neoplasms
/ genetics
CCN Intercellular Signaling Proteins
/ genetics
Cell Line, Tumor
Cell Proliferation
Collagen Type I
/ metabolism
Disease Progression
Female
Gene Expression Regulation, Neoplastic
Humans
Mice
Neoplasm Metastasis
Neoplasm Transplantation
Prognosis
Proto-Oncogene Proteins
/ genetics
Transforming Growth Factor beta1
/ metabolism
Up-Regulation
WISP1
breast cancer
collagen
invasion
metastasis
Journal
The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664
Informations de publication
Date de publication:
15 08 2019
15 08 2019
Historique:
received:
06
12
2018
revised:
13
06
2019
accepted:
19
06
2019
pubmed:
12
7
2019
medline:
24
12
2019
entrez:
12
7
2019
Statut:
ppublish
Résumé
Collagen linearization is a hallmark of aggressive tumors and a key pathogenic event that promotes cancer cell invasion and metastasis. Cell-generated mechanical tension has been proposed to contribute to collagen linearization in tumors, but it is unknown whether other mechanisms play prominent roles in this process. Here, we show that the secretome of cancer cells is by itself able to induce collagen linearization independently of cell-generated mechanical forces. Among the tumor cell-secreted factors, we find a key role in this process for the matricellular protein WISP1 (CCN4). Specifically, WISP1 directly binds to type I collagen to promote its linearization in vitro (in the absence of cells) and in vivo in tumors. Consequently, WISP1-induced type I collagen linearization facilitates tumor cell invasion and promotes spontaneous breast cancer metastasis, without significantly affecting gene expression. Furthermore, higher WISP1 expression in tumors from cancer patients correlates with faster progression to metastatic disease and poor prognosis. Altogether, these findings reveal a conceptually novel mechanism whereby pro-metastatic collagen linearization critically depends on a cancer cell-secreted factor.
Identifiants
pubmed: 31294477
doi: 10.15252/embj.2018101302
pmc: PMC6694215
doi:
Substances chimiques
CCN Intercellular Signaling Proteins
0
CCN4 protein, human
0
Collagen Type I
0
Proto-Oncogene Proteins
0
TGFB1 protein, human
0
Transforming Growth Factor beta1
0
Banques de données
GEO
['GSE110912']
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
e101302Subventions
Organisme : NCI NIH HHS
ID : P30 CA021765
Pays : United States
Organisme : American Lebanese Syrian Associated Charities (ALSAC)
Pays : International
Organisme : HHS|NIH|National Cancer Institute (NCI)
ID : NCI P30 CA021765
Pays : International
Informations de copyright
© 2019 The Authors.
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