Different gDNA content in the subpopulations of prostate cancer extracellular vesicles: Apoptotic bodies, microvesicles, and exosomes

BACKGROUND Extracellular vesicles (EVs) are cell‐derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of their genomic DNA (gDNA) content. It is also unknown whether the DNA cargo is randomly sorted or if it is systematically packed into specific...

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Published in:	The Prostate Vol. 74; no. 14; pp. 1379 - 1390
Main Authors:	Lázaro-Ibáñez, Elisa, Sanz-Garcia, Andres, Visakorpi, Tapio, Escobedo-Lucea, Carmen, Siljander, Pia, Ayuso-Sacido, Ángel, Yliperttula, Marjo
Format:	Journal Article
Language:	English
Published:	United States Blackwell Publishing Ltd 01.10.2014 Wiley Subscription Services, Inc BlackWell Publishing Ltd
Subjects:	Apoptosis - genetics Case-Control Studies Cell Line, Tumor DNA, Neoplasm - genetics DNA, Neoplasm - metabolism Exosomes - genetics Exosomes - metabolism Genes, p53 Humans Male Original Prostatic Neoplasms - blood Prostatic Neoplasms - genetics Prostatic Neoplasms - metabolism Prostatic Neoplasms - pathology PTEN Phosphohydrolase - genetics
ISSN:	0270-4137, 1097-0045, 1097-0045
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Abstract	BACKGROUND Extracellular vesicles (EVs) are cell‐derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of their genomic DNA (gDNA) content. It is also unknown whether the DNA cargo is randomly sorted or if it is systematically packed into specific EV subpopulations. The aim of this study was to analyze whether different prostate cancer (PCa) cell‐derived EV subpopulations (apoptotic bodies, microvesicles, and exosomes) carry different gDNA fragments. METHODS EV subpopulations were isolated from three PCa cell lines (LNCaP, PC‐3, and RC92a/hTERT) and the plasma of PCa patients and healthy donors, and characterized by transmission electron microscopy, nanoparticle tracking analysis and total protein content. gDNA fragments of different genes were detected by real time quantitative PCR and confirmed by DNA sequencing. RESULTS We report that the concentration of EVs was higher in the cancer patients than in the healthy controls. EV subpopulations differed from each other in terms of total protein and DNA content. Analysis of gDNA fragments of MLH1, PTEN, and TP53 genes from the PCa cell‐derived EV subpopulations showed that different EVs carried different gDNA content, which could even harbor specific mutations. Altogether, these results suggest that both nucleic acids and proteins are selectively and cell‐dependently packed into the EV subtypes. CONCLUSIONS EVs derived from PCa cell lines and human plasma samples contain double‐stranded gDNA fragments which could be used to detect specific mutations, making EVs potential biomarkers for cancer diagnostics and prognostics. Prostate 74:1379–1390, 2014. © 2014 The Authors. The Prostate published by Wiley Periodicals, Inc.
AbstractList	Extracellular vesicles (EVs) are cell-derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of their genomic DNA (gDNA) content. It is also unknown whether the DNA cargo is randomly sorted or if it is systematically packed into specific EV subpopulations. The aim of this study was to analyze whether different prostate cancer (PCa) cell-derived EV subpopulations (apoptotic bodies, microvesicles, and exosomes) carry different gDNA fragments.BACKGROUNDExtracellular vesicles (EVs) are cell-derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of their genomic DNA (gDNA) content. It is also unknown whether the DNA cargo is randomly sorted or if it is systematically packed into specific EV subpopulations. The aim of this study was to analyze whether different prostate cancer (PCa) cell-derived EV subpopulations (apoptotic bodies, microvesicles, and exosomes) carry different gDNA fragments.EV subpopulations were isolated from three PCa cell lines (LNCaP, PC-3, and RC92a/hTERT) and the plasma of PCa patients and healthy donors, and characterized by transmission electron microscopy, nanoparticle tracking analysis and total protein content. gDNA fragments of different genes were detected by real time quantitative PCR and confirmed by DNA sequencing.METHODSEV subpopulations were isolated from three PCa cell lines (LNCaP, PC-3, and RC92a/hTERT) and the plasma of PCa patients and healthy donors, and characterized by transmission electron microscopy, nanoparticle tracking analysis and total protein content. gDNA fragments of different genes were detected by real time quantitative PCR and confirmed by DNA sequencing.We report that the concentration of EVs was higher in the cancer patients than in the healthy controls. EV subpopulations differed from each other in terms of total protein and DNA content. Analysis of gDNA fragments of MLH1, PTEN, and TP53 genes from the PCa cell-derived EV subpopulations showed that different EVs carried different gDNA content, which could even harbor specific mutations. Altogether, these results suggest that both nucleic acids and proteins are selectively and cell-dependently packed into the EV subtypes.RESULTSWe report that the concentration of EVs was higher in the cancer patients than in the healthy controls. EV subpopulations differed from each other in terms of total protein and DNA content. Analysis of gDNA fragments of MLH1, PTEN, and TP53 genes from the PCa cell-derived EV subpopulations showed that different EVs carried different gDNA content, which could even harbor specific mutations. Altogether, these results suggest that both nucleic acids and proteins are selectively and cell-dependently packed into the EV subtypes.EVs derived from PCa cell lines and human plasma samples contain double-stranded gDNA fragments which could be used to detect specific mutations, making EVs potential biomarkers for cancer diagnostics and prognostics.CONCLUSIONSEVs derived from PCa cell lines and human plasma samples contain double-stranded gDNA fragments which could be used to detect specific mutations, making EVs potential biomarkers for cancer diagnostics and prognostics. BACKGROUND Extracellular vesicles (EVs) are cell-derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of their genomic DNA (gDNA) content. It is also unknown whether the DNA cargo is randomly sorted or if it is systematically packed into specific EV subpopulations. The aim of this study was to analyze whether different prostate cancer (PCa) cell-derived EV subpopulations (apoptotic bodies, microvesicles, and exosomes) carry different gDNA fragments. METHODS EV subpopulations were isolated from three PCa cell lines (LNCaP, PC-3, and RC92a/hTERT) and the plasma of PCa patients and healthy donors, and characterized by transmission electron microscopy, nanoparticle tracking analysis and total protein content. gDNA fragments of different genes were detected by real time quantitative PCR and confirmed by DNA sequencing. RESULTS We report that the concentration of EVs was higher in the cancer patients than in the healthy controls. EV subpopulations differed from each other in terms of total protein and DNA content. Analysis of gDNA fragments of MLH1, PTEN, and TP53 genes from the PCa cell-derived EV subpopulations showed that different EVs carried different gDNA content, which could even harbor specific mutations. Altogether, these results suggest that both nucleic acids and proteins are selectively and cell-dependently packed into the EV subtypes. CONCLUSIONS EVs derived from PCa cell lines and human plasma samples contain double-stranded gDNA fragments which could be used to detect specific mutations, making EVs potential biomarkers for cancer diagnostics and prognostics. Prostate 74:1379-1390, 2014. © 2014 The Authors. The Prostate published by Wiley Periodicals, Inc. [PUBLICATION ABSTRACT] Extracellular vesicles (EVs) are cell-derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of their genomic DNA (gDNA) content. It is also unknown whether the DNA cargo is randomly sorted or if it is systematically packed into specific EV subpopulations. The aim of this study was to analyze whether different prostate cancer (PCa) cell-derived EV subpopulations (apoptotic bodies, microvesicles, and exosomes) carry different gDNA fragments. EV subpopulations were isolated from three PCa cell lines (LNCaP, PC-3, and RC92a/hTERT) and the plasma of PCa patients and healthy donors, and characterized by transmission electron microscopy, nanoparticle tracking analysis and total protein content. gDNA fragments of different genes were detected by real time quantitative PCR and confirmed by DNA sequencing. We report that the concentration of EVs was higher in the cancer patients than in the healthy controls. EV subpopulations differed from each other in terms of total protein and DNA content. Analysis of gDNA fragments of MLH1, PTEN, and TP53 genes from the PCa cell-derived EV subpopulations showed that different EVs carried different gDNA content, which could even harbor specific mutations. Altogether, these results suggest that both nucleic acids and proteins are selectively and cell-dependently packed into the EV subtypes. EVs derived from PCa cell lines and human plasma samples contain double-stranded gDNA fragments which could be used to detect specific mutations, making EVs potential biomarkers for cancer diagnostics and prognostics. BACKGROUND Extracellular vesicles (EVs) are cell‐derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of their genomic DNA (gDNA) content. It is also unknown whether the DNA cargo is randomly sorted or if it is systematically packed into specific EV subpopulations. The aim of this study was to analyze whether different prostate cancer (PCa) cell‐derived EV subpopulations (apoptotic bodies, microvesicles, and exosomes) carry different gDNA fragments. METHODS EV subpopulations were isolated from three PCa cell lines (LNCaP, PC‐3, and RC92a/hTERT) and the plasma of PCa patients and healthy donors, and characterized by transmission electron microscopy, nanoparticle tracking analysis and total protein content. gDNA fragments of different genes were detected by real time quantitative PCR and confirmed by DNA sequencing. RESULTS We report that the concentration of EVs was higher in the cancer patients than in the healthy controls. EV subpopulations differed from each other in terms of total protein and DNA content. Analysis of gDNA fragments of MLH1, PTEN, and TP53 genes from the PCa cell‐derived EV subpopulations showed that different EVs carried different gDNA content, which could even harbor specific mutations. Altogether, these results suggest that both nucleic acids and proteins are selectively and cell‐dependently packed into the EV subtypes. CONCLUSIONS EVs derived from PCa cell lines and human plasma samples contain double‐stranded gDNA fragments which could be used to detect specific mutations, making EVs potential biomarkers for cancer diagnostics and prognostics. Prostate 74:1379–1390, 2014. © 2014 The Authors. The Prostate published by Wiley Periodicals, Inc.
Author	Siljander, Pia Ayuso-Sacido, Ángel Visakorpi, Tapio Lázaro-Ibáñez, Elisa Yliperttula, Marjo Escobedo-Lucea, Carmen Sanz-Garcia, Andres
Author_xml	– sequence: 1 givenname: Elisa surname: Lázaro-Ibáñez fullname: Lázaro-Ibáñez, Elisa organization: Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Helsinki, Finland – sequence: 2 givenname: Andres surname: Sanz-Garcia fullname: Sanz-Garcia, Andres organization: Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Helsinki, Finland – sequence: 3 givenname: Tapio surname: Visakorpi fullname: Visakorpi, Tapio organization: Institute of Biomedical Technology and BioMediTech, University of Tampere and Tampere University Hospital, Tampere, Finland – sequence: 4 givenname: Carmen surname: Escobedo-Lucea fullname: Escobedo-Lucea, Carmen organization: Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Helsinki, Finland – sequence: 5 givenname: Pia surname: Siljander fullname: Siljander, Pia organization: Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Helsinki, Finland – sequence: 6 givenname: Ángel surname: Ayuso-Sacido fullname: Ayuso-Sacido, Ángel email: marjo.yliperttula@helsinki.fi organization: Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Helsinki, Finland – sequence: 7 givenname: Marjo surname: Yliperttula fullname: Yliperttula, Marjo email: marjo.yliperttula@helsinki.fi organization: Division of Pharmaceutical Biosciences, Faculty of Pharmacy, University of Helsinki, Helsinki, Finland
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25111183$$D View this record in MEDLINE/PubMed
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Copyright	2014 The Authors. published by Wiley Periodicals, Inc. 2014 The Authors. The Prostate published by Wiley Periodicals, Inc. 2014 The Authors. published by Wiley Periodicals, Inc. 2014
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License	Attribution-NonCommercial-NoDerivs http://creativecommons.org/licenses/by-nc-nd/3.0 http://doi.wiley.com/10.1002/tdm_license_1.1 2014 The Authors. The Prostate published by Wiley Periodicals, Inc. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
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Notes	ArticleID:PROS22853 Academy of Finland - No. 259990 Academy of Finland Research Fellow - No. 273689-266486 Finnish Cultural Foundation - No. 00130502 ark:/67375/WNG-F3P7WGZ9-G Carlos III Health Institute - No. PI10/01069; No. CP11/00147 istex:C7B7F9FEA495F8F88F1860A685EBCA77312FA9A2 Magnus Ehrnrooth Foundation Medicinska Understödsföreningen Liv och Hälsa r.f. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Grant sponsor: Finnish Cultural Foundation; Grant number: 00130502; Grant sponsor: Academy of Finland Research Fellow; Grant number: 273689–266486; Grant sponsor: Magnus Ehrnrooth Foundation; Grant sponsor: Medicinska Understödsföreningen Liv och Hälsa r.f.; Grant sponsor: Carlos III Health Institute; Grant numbers: PI10/01069; CP11/00147; Grant sponsor: Academy of Finland; Grant number: 259990.
OpenAccessLink	https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fpros.22853
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PublicationTitle	The Prostate
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Publisher	Blackwell Publishing Ltd Wiley Subscription Services, Inc BlackWell Publishing Ltd
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Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, Bond VC, Borràs FE, Breakefield X, Budnik V, Buzas E, Camussi G, Clayton A, Cocucci E, Falcon-Perez JM, Gabrielsson S, Gho YS, Gupta D, Harsha HC, Hendrix A, Hill AF, Inal JM, Jenster G, Krämer-Albers EM, Lim SK, Llorente A, Lötvall J, Marcilla A, Mincheva-Nilsson L, Nazarenko I, Nieuwland R, Nolte-'t Hoen EN, Pandey A, Patel T, Piper MG, Pluchino S, Prasad TS, Rajendran L, Raposo G, Record M, Reid GE, Sánchez-Madrid F, Schiffelers RM, Siljander P, Stensballe A, Stoorvogel W, Taylor D, Thery C, Valadi H, van Balkom BW, Vázquez J, Vidal M, Wauben MH, Yáñez-Mó M, Zoeller M, Mathivanan S. Vesiclepedia: A compendium for extracellular vesicles with continuous community annotation. PLoS Biol 2012; 10(12):e1001450. Guescini M, Genedani S, Stocchi V, Agnati LF. Astrocytes and glioblastoma cells release exosomes carrying mtDNA. J Neural Transm 2010; 117(1):1-4. Di Vizio D, Kim J, Hager MH, Morello M, Yang W, Lafargue CJ, True LD, Rubin MA, Adam RM, Beroukhim R, Demichelis F, Freeman MR. Oncosome formation in prostate cancer: Association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 2009; 69(13):5601-5609. Peinado H, Alečković M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, García-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, Martins VR, Skog J, Kaplan RN, Brady MS, Wolchok JD, Chapman PB, Kang Y, Bromberg J, Lyden D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012; 18(6):883. Mitchell PJ, Welton J, Staffurth J, Court J, Mason MD, Tabi Z, Clayton A. Can urinary exosomes act as treatment response markers in prostate cancer? J Transl Med 2009; 7:4. D'Souza-Schorey C, Clancy JW. Tumor-derived microvesicles: Shedding light on novel microenvironment modulators and prospective. Cancer Biomarkers 2012; 26(12):1287-1299. Jansen FH, Krijgsveld J, van Rijswijk A, van den Bemd GJ, van den Berg MS, van Weerden WM, Willemsen R, Dekker LJ, Luider TM, Jenster G. Exosomal secretion of cytoplasmic prostate cancer xenograft-derived proteins. Mol Cell Proteomics 2009; 8(6):1192-1205. Bergsmedh A, Szeles A, Henriksson M, Bratt A, Folkman M, Spetz A, Holmgren L. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc Natl Acad Sci USA 2001; 98(11):6407-6411. Hristov M, Erl W, Linder S, Weber PC. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood 2004; 104(9):2761-2766. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10(12):1470-1476. Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, Zhang J, Weitz J, Chin L, Futreal A, Kalluri R. Identification of double stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem 2014; 288(12):26888-26897. Steck PA, Pershouse MA, Jasser SA, Yung WK, Lin H, Ligon AH, Langford LA, Baumgard ML, Hattier T, Davis T, Frye C, Hu R, Swedlund B, Teng DH, Tavtigian SV. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet 1997; 15(4):356-362. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006; 20(5):847-856. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997; 275(5308):1943-1947. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9(6):654-659. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29(6):2001-2007. Nilsson J, Skog J, Nordstrand A, Baranov V, Mincheva-Nilsson L, Breakefield XO, Widmark A. Prostate cancer-derived urine exosomes: A novel approach to biomarkers for prostate cancer. Br J Cancer 2009; 100(10):1603-1607. 2009; 69 2004; 104 2011; 2 2010; 18 1997; 275 2013; 124 2008; 10 2012; 18 2012; 16 2001; 29 2013; 8 2012; 10 2012; 72 2006; 20 2010; 117 1997; 15 2009; 100 2007; 9 2009; 8 2009; 7 2012; 1819 2012; 26 2009; 19 2014; 288 2001; 98 e_1_2_7_6_1 e_1_2_7_5_1 e_1_2_7_3_1 e_1_2_7_8_1 e_1_2_7_7_1 e_1_2_7_19_1 e_1_2_7_18_1 e_1_2_7_17_1 e_1_2_7_16_1 e_1_2_7_2_1 e_1_2_7_14_1 e_1_2_7_13_1 e_1_2_7_12_1 e_1_2_7_11_1 e_1_2_7_10_1 e_1_2_7_26_1 e_1_2_7_27_1 e_1_2_7_28_1 D'Souza‐Schorey C (e_1_2_7_9_1) 2012; 26 Kahlert C (e_1_2_7_25_1) 2014; 288 e_1_2_7_24_1 e_1_2_7_23_1 e_1_2_7_22_1 e_1_2_7_21_1 e_1_2_7_20_1 Pfaffl MW (e_1_2_7_15_1) 2001; 29 Bobrie A (e_1_2_7_4_1) 2012; 16 17486113 - Nat Cell Biol. 2007 Jun;9(6):654-9 20579941 - Cancer Cell. 2010 Jul 13;18(1):11-22 18425114 - Nat Cell Biol. 2008 May;10(5):619-24 22982408 - Biochim Biophys Acta. 2012 Nov-Dec;1819(11-12):1154-63 23936141 - PLoS One. 2013;8(7):e70047 21285958 - Nat Commun. 2011;2:180 15242875 - Blood. 2004 Nov 1;104(9):2761-6 19401683 - Br J Cancer. 2009 May 19;100(10):1603-7 11328886 - Nucleic Acids Res. 2001 May 1;29(9):e45 16453000 - Leukemia. 2006 May;20(5):847-56 24009879 - J Extracell Vesicles. 2012 Apr 16;1:null 23249271 - Clin Sci (Lond). 2013 Apr;124(7):423-41 19011622 - Nat Cell Biol. 2008 Dec;10(12):1470-6 19143024 - Prostate. 2009 May 15;69(7):737-43 23271954 - PLoS Biol. 2012;10(12):e1001450 9072974 - Science. 1997 Mar 28;275(5308):1943-7 24398677 - J Biol Chem. 2014 Feb 14;289(7):3869-75 19138409 - J Transl Med. 2009;7:4 19680595 - J Neural Transm (Vienna). 2010 Jan;117(1):1-4 19549916 - Cancer Res. 2009 Jul 1;69(13):5601-9 19204029 - Mol Cell Proteomics. 2009 Jun;8(6):1192-205 22213130 - Prostate. 2012 Sep 1;72(12):1317-27 19144520 - Trends Cell Biol. 2009 Feb;19(2):43-51 11353826 - Proc Natl Acad Sci U S A. 2001 May 22;98(11):6407-11 9090379 - Nat Genet. 1997 Apr;15(4):356-62 22713869 - Genes Dev. 2012 Jun 15;26(12):1287-99 22635005 - Nat Med. 2012 Jun;18(6):883-91
References_xml	– reference: Jansen FH, Krijgsveld J, van Rijswijk A, van den Bemd GJ, van den Berg MS, van Weerden WM, Willemsen R, Dekker LJ, Luider TM, Jenster G. Exosomal secretion of cytoplasmic prostate cancer xenograft-derived proteins. Mol Cell Proteomics 2009; 8(6):1192-1205. – reference: Burger D, Schock S, Thompson CS, Montezano AC, Hakim AM, Touyz RM. Microparticles: Biomarkers and beyond. Clin Sci 2013; 124(7-8):423-441. – reference: Bobrie A, Colombo M, Krumeich S, Raposo G, Thery C. Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation. Journal of Extracellular Vesicles 2012; 16:1. – reference: Mitchell PJ, Welton J, Staffurth J, Court J, Mason MD, Tabi Z, Clayton A. Can urinary exosomes act as treatment response markers in prostate cancer? J Transl Med 2009; 7:4. – reference: Peinado H, Alečković M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, García-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, Martins VR, Skog J, Kaplan RN, Brady MS, Wolchok JD, Chapman PB, Kang Y, Bromberg J, Lyden D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012; 18(6):883. – reference: Nilsson J, Skog J, Nordstrand A, Baranov V, Mincheva-Nilsson L, Breakefield XO, Widmark A. Prostate cancer-derived urine exosomes: A novel approach to biomarkers for prostate cancer. Br J Cancer 2009; 100(10):1603-1607. – reference: Ronquist KG, Ronquist G, Carlsson L, Larsson A. Human prostasomes contain chromosomal DNA. Prostate 2009; 69(7):737-743. – reference: Hristov M, Erl W, Linder S, Weber PC. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood 2004; 104(9):2761-2766. – reference: Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10(12):1470-1476. – reference: Guescini M, Genedani S, Stocchi V, Agnati LF. Astrocytes and glioblastoma cells release exosomes carrying mtDNA. J Neural Transm 2010; 117(1):1-4. – reference: Hessvik NP, Phuyal S, Brech A, Sandvig K, Llorente A. Profiling of microRNAs in exosomes released from PC-3 prostate cancer cells. Biochim Biophys Acta 2012; 1819(11-12):1154-1163. – reference: Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: Artefacts no more. Trends Cell Biol 2009; 19(2):43-51. – reference: Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006; 20(5):847-856. – reference: Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, Skog J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011; 2:180. – reference: Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, Bond VC, Borràs FE, Breakefield X, Budnik V, Buzas E, Camussi G, Clayton A, Cocucci E, Falcon-Perez JM, Gabrielsson S, Gho YS, Gupta D, Harsha HC, Hendrix A, Hill AF, Inal JM, Jenster G, Krämer-Albers EM, Lim SK, Llorente A, Lötvall J, Marcilla A, Mincheva-Nilsson L, Nazarenko I, Nieuwland R, Nolte-'t Hoen EN, Pandey A, Patel T, Piper MG, Pluchino S, Prasad TS, Rajendran L, Raposo G, Record M, Reid GE, Sánchez-Madrid F, Schiffelers RM, Siljander P, Stensballe A, Stoorvogel W, Taylor D, Thery C, Valadi H, van Balkom BW, Vázquez J, Vidal M, Wauben MH, Yáñez-Mó M, Zoeller M, Mathivanan S. Vesiclepedia: A compendium for extracellular vesicles with continuous community annotation. PLoS Biol 2012; 10(12):e1001450. – reference: Steck PA, Pershouse MA, Jasser SA, Yung WK, Lin H, Ligon AH, Langford LA, Baumgard ML, Hattier T, Davis T, Frye C, Hu R, Swedlund B, Teng DH, Tavtigian SV. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet 1997; 15(4):356-362. – reference: Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, Antipin Y, Mitsiades N, Landers T, Dolgalev I, Major JE, Wilson M, Socci ND, Lash AE, Heguy A, Eastham JA, Scher HI, Reuter VE, Scardino PT, Sander C, Sawyers CL, Gerald WL. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010; 18(1):11-22. – reference: Di Vizio D, Kim J, Hager MH, Morello M, Yang W, Lafargue CJ, True LD, Rubin MA, Adam RM, Beroukhim R, Demichelis F, Freeman MR. Oncosome formation in prostate cancer: Association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 2009; 69(13):5601-5609. – reference: Spans L, Atak ZK, Van Nieuwerburgh F, Deforce D, Lerut E, Aerts S, Claessens F. Variations in the exome of the LNCaP prostate cancer cell line. Prostate 2012; 72(12):1317-1327. – reference: Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, Zhang J, Weitz J, Chin L, Futreal A, Kalluri R. Identification of double stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem 2014; 288(12):26888-26897. – reference: D'Souza-Schorey C, Clancy JW. Tumor-derived microvesicles: Shedding light on novel microenvironment modulators and prospective. Cancer Biomarkers 2012; 26(12):1287-1299. – reference: Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29(6):2001-2007. – reference: Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, Rak J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008; 10(5):619-624. – reference: Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997; 275(5308):1943-1947. – reference: Bergsmedh A, Szeles A, Henriksson M, Bratt A, Folkman M, Spetz A, Holmgren L. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc Natl Acad Sci USA 2001; 98(11):6407-6411. – reference: Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9(6):654-659. – reference: Gabriel K, Ingram A, Austin R, Kapoor A, Tang D, Majeed F, Qureshi T, Al-Nedawi K. Regulation of the tumor suppressor PTEN through exosomes: A diagnostic potential for prostate cancer. PLoS ONE 2013; 8(7):e70047. – volume: 2 start-page: 180 year: 2011 article-title: Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences publication-title: Nat Commun – volume: 18 start-page: 883 issue: 6 year: 2012 article-title: Melanoma exosomes educate bone marrow progenitor cells toward a pro‐metastatic phenotype through MET publication-title: Nat Med – volume: 26 start-page: 1287 issue: 12 year: 2012 end-page: 1299 article-title: Tumor‐derived microvesicles: Shedding light on novel microenvironment modulators and prospective publication-title: Cancer Biomarkers – volume: 18 start-page: 11 issue: 1 year: 2010 end-page: 22 article-title: Integrative genomic profiling of human prostate cancer publication-title: Cancer Cell – volume: 8 start-page: e70047 issue: 7 year: 2013 article-title: Regulation of the tumor suppressor PTEN through exosomes: A diagnostic potential for prostate cancer publication-title: PLoS ONE – volume: 288 start-page: 26888 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Snippet	BACKGROUND Extracellular vesicles (EVs) are cell‐derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of... Extracellular vesicles (EVs) are cell-derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of their... BACKGROUND Extracellular vesicles (EVs) are cell-derived membrane vesicles. EVs contain several RNAs such as mRNA, microRNAs, and ncRNAs, but less is known of...
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SubjectTerms	Apoptosis - genetics Case-Control Studies Cell Line, Tumor DNA, Neoplasm - genetics DNA, Neoplasm - metabolism Exosomes - genetics Exosomes - metabolism Genes, p53 Humans Male Original Prostatic Neoplasms - blood Prostatic Neoplasms - genetics Prostatic Neoplasms - metabolism Prostatic Neoplasms - pathology PTEN Phosphohydrolase - genetics
Title	Different gDNA content in the subpopulations of prostate cancer extracellular vesicles: Apoptotic bodies, microvesicles, and exosomes
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