Subpopulations of extracellular vesicles from human metastatic melanoma tissue identified by quantitative proteomics after optimized isolation

The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs in vivo. The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated direct...

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Published inJournal of extracellular vesicles Vol. 9; no. 1; pp. 1722433 - n/a
Main Authors Crescitelli, Rossella, Lässer, Cecilia, Jang, Su Chul, Cvjetkovic, Aleksander, Malmhäll, Carina, Karimi, Nasibeh, Höög, Johanna L., Johansson, Iva, Fuchs, Johannes, Thorsell, Annika, Gho, Yong Song, Olofsson Bagge, R., Lötvall, Jan
Format Journal Article
LanguageEnglish
Published Sweden Taylor & Francis 01.01.2020
John Wiley & Sons, Inc
Wiley
Subjects
Antibodies
Biomarkers
Biotechnology
Cell Biology
Cells
Clinical Medicine
Cloning
Collagenase
Deoxyribonuclease
Electron microscopy
endocytosis
exosomes
Extracellular vesicles
Flow cytometry
Klinisk medicin
malignant-melanoma
markers
mass spectrometry
Mass spectroscopy
Melanoma
membrane-vesicles
Metastases
Metastasis
micrornas
microvesicles
Nanoparticles
Physical characteristics
Proteomics
Ribosomal subunits
rme-8
rRNA 18S
rRNA 28S
Skin cancer
subpopulations
tag
tandem mass
tandem mass tag
tissue-derived vesicles
transferrin receptor
Tumor cell lines
Tumors
Ultracentrifugation
vesicle isolation
visualization
Sweden
Japan
Germany
tandem mass tag
exosomes
subpopulations
tissue-derived vesicles
Extracellular vesicles
mass spectrometry
melanoma
vesicle isolation
microvesicles
Online AccessGet full text

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Abstract The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs in vivo. The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low-density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer®, nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin-1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.
AbstractList The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs in vivo. The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low-density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer®, nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin-1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.
The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs  in vivo . The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low‐density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer®, nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin‐1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.
ABSTRACT The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs in vivo. The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low‐density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer®, nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin‐1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.
The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs  . The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low-density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer®, nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin-1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.
The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs in vivo. The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low-density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer (R), nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin-1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.
ABSTRACT The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs in vivo. The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low‐density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer®, nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin‐1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.
The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs in vivo. The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low-density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer®, nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin-1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the characteristics of EVs in vivo. The aim of this study was to establish a method to isolate and categorize subpopulations of EVs isolated directly from tumour tissue. First we established an isolation protocol for subpopulations of EVs from metastatic melanoma tissue, which included enzymatic treatment (collagenase D and DNase). Small and large EVs were isolated with differential ultracentrifugation, and these were further separated into high and low-density (HD and LD) fractions. All EV subpopulations were then analysed in depth using electron microscopy, Bioanalyzer®, nanoparticle tracking analysis, and quantitative mass spectrometry analysis. Subpopulations of EVs with distinct size, morphology, and RNA and protein cargo could be isolated from the metastatic melanoma tissue. LD EVs showed an RNA profile with the presence of 18S and 28S ribosomal subunits. In contrast, HD EVs had RNA profiles with small or no peaks for ribosomal RNA subunits. Quantitative proteomics showed that several proteins such as flotillin-1 were enriched in both large and small LD EVs, while ADAM10 were exclusively enriched in small LD EVs. In contrast, mitofilin was enriched only in the large EVs. We conclude that enzymatic treatments improve EV isolation from dense fibrotic tissue without any apparent effect on molecular or morphological characteristics. By providing a detailed categorization of several subpopulations of EVs isolated directly from tumour tissues, we might better understand the function of EVs in tumour biology and their possible use in biomarker discovery.
Author Malmhäll, Carina
Lötvall, Jan
Cvjetkovic, Aleksander
Johansson, Iva
Lässer, Cecilia
Gho, Yong Song
Jang, Su Chul
Höög, Johanna L.
Fuchs, Johannes
Thorsell, Annika
Crescitelli, Rossella
Olofsson Bagge, R.
Karimi, Nasibeh
Author_xml – sequence: 1
  givenname: Rossella
  orcidid: 0000-0002-1714-3169
  surname: Crescitelli
  fullname: Crescitelli, Rossella
  organization: Institute of Medicine Sahlgrenska Academy at University of Gothenburg
– sequence: 2
  givenname: Cecilia
  orcidid: 0000-0003-1279-1746
  surname: Lässer
  fullname: Lässer, Cecilia
  email: cecilia.lasser@gu.se
  organization: Institute of Medicine Sahlgrenska Academy at University of Gothenburg
– sequence: 3
  givenname: Su Chul
  orcidid: 0000-0003-3326-1007
  surname: Jang
  fullname: Jang, Su Chul
  organization: Institute of Medicine Sahlgrenska Academy at University of Gothenburg
– sequence: 4
  givenname: Aleksander
  orcidid: 0000-0002-9131-9791
  surname: Cvjetkovic
  fullname: Cvjetkovic, Aleksander
  organization: Institute of Medicine Sahlgrenska Academy at University of Gothenburg
– sequence: 5
  givenname: Carina
  surname: Malmhäll
  fullname: Malmhäll, Carina
  organization: Institute of Medicine Sahlgrenska Academy at University of Gothenburg
– sequence: 6
  givenname: Nasibeh
  surname: Karimi
  fullname: Karimi, Nasibeh
  organization: Institute of Medicine Sahlgrenska Academy at University of Gothenburg
– sequence: 7
  givenname: Johanna L.
  surname: Höög
  fullname: Höög, Johanna L.
  organization: University of Gothenburg
– sequence: 8
  givenname: Iva
  orcidid: 0000-0003-2162-3816
  surname: Johansson
  fullname: Johansson, Iva
  organization: Sahlgrenska University Hospital
– sequence: 9
  givenname: Johannes
  surname: Fuchs
  fullname: Fuchs, Johannes
  organization: Sahlgrenska Academy at University of Gothenburg
– sequence: 10
  givenname: Annika
  surname: Thorsell
  fullname: Thorsell, Annika
  organization: Sahlgrenska Academy at University of Gothenburg
– sequence: 11
  givenname: Yong Song
  surname: Gho
  fullname: Gho, Yong Song
  organization: Pohang University of Science and Technology
– sequence: 12
  givenname: R.
  orcidid: 0000-0001-5795-0355
  surname: Olofsson Bagge
  fullname: Olofsson Bagge, R.
  organization: University of Gothenburg
– sequence: 13
  givenname: Jan
  orcidid: 0000-0001-9195-9249
  surname: Lötvall
  fullname: Lötvall, Jan
  email: jan.lotvall@gu.se
  organization: Institute of Medicine Sahlgrenska Academy at University of Gothenburg
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32128073$$D View this record in MEDLINE/PubMed
https://gup.ub.gu.se/publication/291542$$DView record from Swedish Publication Index
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Issue 1
Keywords tandem mass tag
exosomes
subpopulations
tissue-derived vesicles
Extracellular vesicles
mass spectrometry
melanoma
vesicle isolation
microvesicles
Language English
License open-access: http://creativecommons.org/licenses/by/4.0/: http://creativecommons.org/licenses/by/4.0/: This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Attribution
http://creativecommons.org/licenses/by/4.0
2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group on behalf of The International Society for Extracellular Vesicles.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Snippet The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these represent the...
ABSTRACT The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these...
ABSTRACT The majority of extracellular vesicle (EV) studies conducted to date have been performed on cell lines with little knowledge on how well these...
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SubjectTerms Antibodies
Biomarkers
Biotechnology
Cell Biology
Cells
Clinical Medicine
Cloning
Collagenase
Deoxyribonuclease
Electron microscopy
endocytosis
exosomes
Extracellular vesicles
Flow cytometry
Klinisk medicin
malignant-melanoma
markers
mass spectrometry
Mass spectroscopy
Melanoma
membrane-vesicles
Metastases
Metastasis
micrornas
microvesicles
Nanoparticles
Physical characteristics
Proteomics
Ribosomal subunits
rme-8
rRNA 18S
rRNA 28S
Skin cancer
subpopulations
tag
tandem mass
tandem mass tag
tissue-derived vesicles
transferrin receptor
Tumor cell lines
Tumors
Ultracentrifugation
vesicle isolation
visualization
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Title Subpopulations of extracellular vesicles from human metastatic melanoma tissue identified by quantitative proteomics after optimized isolation
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Volume 9
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