A role of tumor-released exosomes in paracrine dissemination and metastasis

E.P. Spugnini, M. Logozzi, R. Di Raimo, D. Mizzoni, S. Fais

Research output: Contribution to journalArticle

Abstract

Metastatic diffusion is thought to be a multi-step phenomenon involving the release of cells from the primary tumor and their diffusion through the body. Currently, several hypotheses have been put forward in order to explain the origin of cancer metastasis, including epithelial–mesenchymal transition, mutagenesis of stem cells, and a facilitating role of macrophages, involving, for example, transformation or fusion hybridization with neoplastic cells. In this paradigm, tumor-secreted extracellular vesicles (EVs), such as exosomes, play a pivotal role in cell communications, delivering a plethora of biomolecules including proteins, lipids, and nucleic acids. For their natural role in shuttling molecules, EVs have been newly considered a part of the metastatic cascade. They have a prominent role in preparing the so-called “tumor niches” in target organs. However, recent evidence has pointed out an even more interesting role of tumor EVs, consisting in their ability to induce malignant transformation in resident mesenchymal stem cells. All in all, in this review, we discuss the multiple involvements of EVs in the metastatic cascade, and how we can exploit and manipulate EVs in order to reduce the metastatic spread of malignant tumors. © 2018 by the authors. Licensee MDPI, Basel, Switzerland.
Original languageEnglish
JournalInternational Journal of Molecular Sciences
Volume19
Issue number12
DOIs
Publication statusPublished - 2018

Fingerprint

Exosomes
metastasis
Tumors
tumors
Neoplasm Metastasis
stem cells
Neoplasms
Stem cells
cascades
cells
mutagenesis
Mutagenesis
acids
macrophages
Macrophages
Nucleic acids
Biomolecules
nucleic acids
Switzerland
organs

Keywords

  • Cell-free DNA
  • Exosomes
  • Extracellular vesicles
  • Metastasis
  • Metastatic niche
  • Tumor microenvironment
  • microRNA
  • small interfering RNA
  • vasculotropin
  • apoptosis
  • carcinogenesis
  • cardiovascular disease
  • enzyme linked immunosorbent assay
  • human
  • hypoxia
  • immune response
  • liquid biopsy
  • nonhuman
  • oxidative stress
  • paracrine signaling
  • pleura effusion
  • Review
  • tumor growth
  • tumor microenvironment

Cite this

A role of tumor-released exosomes in paracrine dissemination and metastasis. / Spugnini, E.P.; Logozzi, M.; Di Raimo, R.; Mizzoni, D.; Fais, S.

In: International Journal of Molecular Sciences, Vol. 19, No. 12, 2018.

Research output: Contribution to journalArticle

@article{474ce2e6a49f43babb12e1867cacba29,
title = "A role of tumor-released exosomes in paracrine dissemination and metastasis",
abstract = "Metastatic diffusion is thought to be a multi-step phenomenon involving the release of cells from the primary tumor and their diffusion through the body. Currently, several hypotheses have been put forward in order to explain the origin of cancer metastasis, including epithelial–mesenchymal transition, mutagenesis of stem cells, and a facilitating role of macrophages, involving, for example, transformation or fusion hybridization with neoplastic cells. In this paradigm, tumor-secreted extracellular vesicles (EVs), such as exosomes, play a pivotal role in cell communications, delivering a plethora of biomolecules including proteins, lipids, and nucleic acids. For their natural role in shuttling molecules, EVs have been newly considered a part of the metastatic cascade. They have a prominent role in preparing the so-called “tumor niches” in target organs. However, recent evidence has pointed out an even more interesting role of tumor EVs, consisting in their ability to induce malignant transformation in resident mesenchymal stem cells. All in all, in this review, we discuss the multiple involvements of EVs in the metastatic cascade, and how we can exploit and manipulate EVs in order to reduce the metastatic spread of malignant tumors. {\circledC} 2018 by the authors. Licensee MDPI, Basel, Switzerland.",
keywords = "Cell-free DNA, Exosomes, Extracellular vesicles, Metastasis, Metastatic niche, Tumor microenvironment, microRNA, small interfering RNA, vasculotropin, apoptosis, carcinogenesis, cardiovascular disease, enzyme linked immunosorbent assay, human, hypoxia, immune response, liquid biopsy, nonhuman, oxidative stress, paracrine signaling, pleura effusion, Review, tumor growth, tumor microenvironment",
author = "E.P. Spugnini and M. Logozzi and {Di Raimo}, R. and D. Mizzoni and S. Fais",
note = "Cited By :1 Export Date: 11 April 2019 Correspondence Address: Fais, S.; Department of Oncology and Molecular Medicine, National Institute of Health, Viale Regina Elena 299, Italy; email: stefano.fais@iss.it Chemicals/CAS: vasculotropin, 127464-60-2 Funding details: Foundation for the National Institutes of Health, 15ONC/5 Funding text 1: Funding: This work was supported by a grant from the Italian Ministry of Health (National Institute of Health internal classification: 15ONC/5). References: Liu, W., Vivian, C.J., Brinker, A.E., Hampton, K.R., Lianidou, E., Welch, D.R., Microenvironmental Influences on Metastasis Suppressor Expression and Function during a Metastatic Cell’s Journey (2014) Cancer Microenviron, 7, pp. 117-131; Nogu{\'e}s, L., Benito-Martin, A., Hergueta-Redondo, M., Peinado, H., The influence of tumour-derived extracellular vesicles on local and distal metastatic dissemination (2018) Mol. 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year = "2018",
doi = "10.3390/ijms19123968",
language = "English",
volume = "19",
journal = "International Journal of Molecular Sciences",
issn = "1661-6596",
publisher = "MDPI AG",
number = "12",

}

TY - JOUR

T1 - A role of tumor-released exosomes in paracrine dissemination and metastasis

AU - Spugnini, E.P.

AU - Logozzi, M.

AU - Di Raimo, R.

AU - Mizzoni, D.

AU - Fais, S.

N1 - Cited By :1 Export Date: 11 April 2019 Correspondence Address: Fais, S.; Department of Oncology and Molecular Medicine, National Institute of Health, Viale Regina Elena 299, Italy; email: stefano.fais@iss.it Chemicals/CAS: vasculotropin, 127464-60-2 Funding details: Foundation for the National Institutes of Health, 15ONC/5 Funding text 1: Funding: This work was supported by a grant from the Italian Ministry of Health (National Institute of Health internal classification: 15ONC/5). References: Liu, W., Vivian, C.J., Brinker, A.E., Hampton, K.R., Lianidou, E., Welch, D.R., Microenvironmental Influences on Metastasis Suppressor Expression and Function during a Metastatic Cell’s Journey (2014) Cancer Microenviron, 7, pp. 117-131; Nogués, L., Benito-Martin, A., Hergueta-Redondo, M., Peinado, H., The influence of tumour-derived extracellular vesicles on local and distal metastatic dissemination (2018) Mol. 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PY - 2018

Y1 - 2018

N2 - Metastatic diffusion is thought to be a multi-step phenomenon involving the release of cells from the primary tumor and their diffusion through the body. Currently, several hypotheses have been put forward in order to explain the origin of cancer metastasis, including epithelial–mesenchymal transition, mutagenesis of stem cells, and a facilitating role of macrophages, involving, for example, transformation or fusion hybridization with neoplastic cells. In this paradigm, tumor-secreted extracellular vesicles (EVs), such as exosomes, play a pivotal role in cell communications, delivering a plethora of biomolecules including proteins, lipids, and nucleic acids. For their natural role in shuttling molecules, EVs have been newly considered a part of the metastatic cascade. They have a prominent role in preparing the so-called “tumor niches” in target organs. However, recent evidence has pointed out an even more interesting role of tumor EVs, consisting in their ability to induce malignant transformation in resident mesenchymal stem cells. All in all, in this review, we discuss the multiple involvements of EVs in the metastatic cascade, and how we can exploit and manipulate EVs in order to reduce the metastatic spread of malignant tumors. © 2018 by the authors. Licensee MDPI, Basel, Switzerland.

AB - Metastatic diffusion is thought to be a multi-step phenomenon involving the release of cells from the primary tumor and their diffusion through the body. Currently, several hypotheses have been put forward in order to explain the origin of cancer metastasis, including epithelial–mesenchymal transition, mutagenesis of stem cells, and a facilitating role of macrophages, involving, for example, transformation or fusion hybridization with neoplastic cells. In this paradigm, tumor-secreted extracellular vesicles (EVs), such as exosomes, play a pivotal role in cell communications, delivering a plethora of biomolecules including proteins, lipids, and nucleic acids. For their natural role in shuttling molecules, EVs have been newly considered a part of the metastatic cascade. They have a prominent role in preparing the so-called “tumor niches” in target organs. However, recent evidence has pointed out an even more interesting role of tumor EVs, consisting in their ability to induce malignant transformation in resident mesenchymal stem cells. All in all, in this review, we discuss the multiple involvements of EVs in the metastatic cascade, and how we can exploit and manipulate EVs in order to reduce the metastatic spread of malignant tumors. © 2018 by the authors. Licensee MDPI, Basel, Switzerland.

KW - Cell-free DNA

KW - Exosomes

KW - Extracellular vesicles

KW - Metastasis

KW - Metastatic niche

KW - Tumor microenvironment

KW - microRNA

KW - small interfering RNA

KW - vasculotropin

KW - apoptosis

KW - carcinogenesis

KW - cardiovascular disease

KW - enzyme linked immunosorbent assay

KW - human

KW - hypoxia

KW - immune response

KW - liquid biopsy

KW - nonhuman

KW - oxidative stress

KW - paracrine signaling

KW - pleura effusion

KW - Review

KW - tumor growth

KW - tumor microenvironment

U2 - 10.3390/ijms19123968

DO - 10.3390/ijms19123968

M3 - Article

VL - 19

JO - International Journal of Molecular Sciences

JF - International Journal of Molecular Sciences

SN - 1661-6596

IS - 12

ER -