Periostin is a key niche component for wound metastasis of melanoma

Keitaro Fukuda, Eiji Sugihara, Shoichiro Ohta, Kenji Izuhara, Takeru Funakoshi, Masayuki Amagai, Hideyuki Saya

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Tissue injury promotes metastasis of several human cancers, although factors associated with wound healing that attract circulating tumor cells have remained unknown. Here, we examined the primary and metastatic lesions that appeared 1 month after trauma in a patient with acral lentiginous melanoma. The levels of mRNA for periostin (POSTN), type 1 collagen, and fibronectin were significantly increased in the metastatic lesion relative to the primary lesion. The increase of these extracellular matrix proteins at the wound site was reproduced in a mouse model of wound healing, with the upregulation of Postn mRNA persisting the longest. POSTN was expressed in the region surrounding melanoma cell nests in metastatic lesions of both wounded mice and the patient. POSTN attenuated the cell adhesion and promoted the migration of melanoma cells without affecting their proliferation in vitro. In the mouse model, the wound site as well as subcutaneously injected osteoblasts that secrete large amounts of POSTN invited the metastasis of remotely-transplanted melanoma cells on the sites. Osteoblasts with suppression of POSTN by shRNA showed a greatly reduced ability to promote such metastasis. Our results suggest that POSTN is a key factor in promoting melanoma cell metastasis to wound sites by providing a premetastatic niche.

Original languageEnglish
Article numbere0129704
JournalPLoS One
Volume10
Issue number6
DOIs
Publication statusPublished - 2015 Jun 17

Fingerprint

Osteoblasts
melanoma
animal injuries
metastasis
Melanoma
niches
lesions (animal)
Neoplasm Metastasis
Messenger RNA
Extracellular Matrix Proteins
Cell adhesion
Wounds and Injuries
Collagen Type I
Fibronectins
osteoblasts
Small Interfering RNA
Tumors
tissue repair
Wound Healing
Cells

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Periostin is a key niche component for wound metastasis of melanoma. / Fukuda, Keitaro; Sugihara, Eiji; Ohta, Shoichiro; Izuhara, Kenji; Funakoshi, Takeru; Amagai, Masayuki; Saya, Hideyuki.

In: PLoS One, Vol. 10, No. 6, e0129704, 17.06.2015.

Research output: Contribution to journalArticle

Fukuda, Keitaro ; Sugihara, Eiji ; Ohta, Shoichiro ; Izuhara, Kenji ; Funakoshi, Takeru ; Amagai, Masayuki ; Saya, Hideyuki. / Periostin is a key niche component for wound metastasis of melanoma. In: PLoS One. 2015 ; Vol. 10, No. 6.
@article{1631c1aab0114bc88b263193a27d5b2f,
title = "Periostin is a key niche component for wound metastasis of melanoma",
abstract = "Tissue injury promotes metastasis of several human cancers, although factors associated with wound healing that attract circulating tumor cells have remained unknown. Here, we examined the primary and metastatic lesions that appeared 1 month after trauma in a patient with acral lentiginous melanoma. The levels of mRNA for periostin (POSTN), type 1 collagen, and fibronectin were significantly increased in the metastatic lesion relative to the primary lesion. The increase of these extracellular matrix proteins at the wound site was reproduced in a mouse model of wound healing, with the upregulation of Postn mRNA persisting the longest. POSTN was expressed in the region surrounding melanoma cell nests in metastatic lesions of both wounded mice and the patient. POSTN attenuated the cell adhesion and promoted the migration of melanoma cells without affecting their proliferation in vitro. In the mouse model, the wound site as well as subcutaneously injected osteoblasts that secrete large amounts of POSTN invited the metastasis of remotely-transplanted melanoma cells on the sites. Osteoblasts with suppression of POSTN by shRNA showed a greatly reduced ability to promote such metastasis. Our results suggest that POSTN is a key factor in promoting melanoma cell metastasis to wound sites by providing a premetastatic niche.",
author = "Keitaro Fukuda and Eiji Sugihara and Shoichiro Ohta and Kenji Izuhara and Takeru Funakoshi and Masayuki Amagai and Hideyuki Saya",
year = "2015",
month = "6",
day = "17",
doi = "10.1371/journal.pone.0129704",
language = "English",
volume = "10",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "6",

}

TY - JOUR

T1 - Periostin is a key niche component for wound metastasis of melanoma

AU - Fukuda, Keitaro

AU - Sugihara, Eiji

AU - Ohta, Shoichiro

AU - Izuhara, Kenji

AU - Funakoshi, Takeru

AU - Amagai, Masayuki

AU - Saya, Hideyuki

PY - 2015/6/17

Y1 - 2015/6/17

N2 - Tissue injury promotes metastasis of several human cancers, although factors associated with wound healing that attract circulating tumor cells have remained unknown. Here, we examined the primary and metastatic lesions that appeared 1 month after trauma in a patient with acral lentiginous melanoma. The levels of mRNA for periostin (POSTN), type 1 collagen, and fibronectin were significantly increased in the metastatic lesion relative to the primary lesion. The increase of these extracellular matrix proteins at the wound site was reproduced in a mouse model of wound healing, with the upregulation of Postn mRNA persisting the longest. POSTN was expressed in the region surrounding melanoma cell nests in metastatic lesions of both wounded mice and the patient. POSTN attenuated the cell adhesion and promoted the migration of melanoma cells without affecting their proliferation in vitro. In the mouse model, the wound site as well as subcutaneously injected osteoblasts that secrete large amounts of POSTN invited the metastasis of remotely-transplanted melanoma cells on the sites. Osteoblasts with suppression of POSTN by shRNA showed a greatly reduced ability to promote such metastasis. Our results suggest that POSTN is a key factor in promoting melanoma cell metastasis to wound sites by providing a premetastatic niche.

AB - Tissue injury promotes metastasis of several human cancers, although factors associated with wound healing that attract circulating tumor cells have remained unknown. Here, we examined the primary and metastatic lesions that appeared 1 month after trauma in a patient with acral lentiginous melanoma. The levels of mRNA for periostin (POSTN), type 1 collagen, and fibronectin were significantly increased in the metastatic lesion relative to the primary lesion. The increase of these extracellular matrix proteins at the wound site was reproduced in a mouse model of wound healing, with the upregulation of Postn mRNA persisting the longest. POSTN was expressed in the region surrounding melanoma cell nests in metastatic lesions of both wounded mice and the patient. POSTN attenuated the cell adhesion and promoted the migration of melanoma cells without affecting their proliferation in vitro. In the mouse model, the wound site as well as subcutaneously injected osteoblasts that secrete large amounts of POSTN invited the metastasis of remotely-transplanted melanoma cells on the sites. Osteoblasts with suppression of POSTN by shRNA showed a greatly reduced ability to promote such metastasis. Our results suggest that POSTN is a key factor in promoting melanoma cell metastasis to wound sites by providing a premetastatic niche.

UR - http://www.scopus.com/inward/record.url?scp=84939125072&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84939125072&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0129704

DO - 10.1371/journal.pone.0129704

M3 - Article

VL - 10

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 6

M1 - e0129704

ER -