2,078
Views
16
CrossRef citations to date
0
Altmetric
Research Article

Profiling plasma extracellular vesicle by pluronic block-copolymer based enrichment method unveils features associated with breast cancer aggression, metastasis and invasion

ORCID Icon, , &
Article: 1458574 | Received 03 Dec 2017, Accepted 17 Mar 2018, Published online: 05 Apr 2018

References

  • Orozco AF, Lewis DE. Flow cytometric analysis of circulating microparticles in plasma. Cytometry A. 2010;77:1–23.
  • Stoorvogel W, Kleijmeer MJ, Geuze HJ, et al. The biogenesis and functions of exosomes. Traffic. 2002;3:321–330.
  • Livshits MA, Khomyakova E, Evtushenko EG, et al. Isolation of exosomes by differential centrifugation: theoretical analysis of a commonly used protocol. Sci Rep. 2015;5:17319.
  • Thery C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;30 (1):3.22.1–3.22.29.
  • Antes TJ, Kwei K. Methods for microvesicle isolation and selective removal. System Biosciences LLC, US20130337440A1; 2013.
  • Helwa I, Cai J, Drewry MD, et al. A comparative study of serum exosome isolation using differential ultracentrifugation and three commercial reagents. PLoS One. 2017;12:e0170628.
  • Caradec J, Kharmate G, Hosseini-Beheshti E, et al. Reproducibility and efficiency of serum-derived exosome extraction methods. Clin Biochem. 2014;47:1286–1292.
  • Van Deun J, Mestdagh P, Sormunen R, et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles. 2014;32858.
  • Kabanov AV, Lemieux P, Vinogradov S, et al. Pluronic block copolymers: novel functional molecules for gene therapy. Adv Drug Deliv Rev. 2002;54:223–233.
  • Shelat PB, Plant LD, Wang JC, et al. The membrane-active tri-block copolymer pluronic F-68 profoundly rescues rat hippocampal neurons from oxygen-glucose deprivation-induced death through early inhibition of apoptosis. J Neurosci. 2013;33:12287–12299.
  • Firestone MA, Wolf AC, Seifert S. Small-angle X-ray scattering study of the interaction of poly(ethylene oxide)-b-poly(propylene oxide)-b-poly(ethylene oxide) triblock copolymers with lipid bilayers. Biomacromolecules. 2003;4:1539–1549.
  • Lee RC, River LP, Pan FS, et al. Surfactant-induced sealing of electropermeabilized skeletal muscle membranes in vivo. Proc Natl Acad Sci U S A. 1992;89:4524–4528.
  • Marks JD, Pan CY, Bushell T, et al. Amphiphilic, tri-block copolymers provide potent membrane-targeted neuroprotection. Faseb J. 2001;15:1107–1109.
  • Melnichenko AA, Aksenov DV, Myasoedova VA, et al. Pluronic block copolymers inhibit low density lipoprotein self-association. Lipids. 2012;47:995–1000.
  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–675.
  • Trapnell C, Williams BA, Pertea G, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511–515.
  • Rekker K, Saare M, Roost AM, et al. Circulating microRNA Profile throughout the menstrual cycle. PLoS One. 2013;8:e81166.
  • Chambers MC, Maclean B, Burke R, et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol. 2012;30:918–920.
  • Kim S, Pevzner PA. MS-GF+ makes progress towards a universal database search tool for proteomics. Nat Commun. 2014;5:5277.
  • Krey JF, Wilmarth PA, Shin JB, et al. Accurate label-free protein quantitation with high- and low-resolution mass spectrometers. J Proteome Res. 2014;13:1034–1044.
  • Sardiu ME, Washburn MP. Enriching quantitative proteomics with SI(N). Nat Biotechnol. 2010;28:40–42.
  • Lotvall J, Hill AF, Hochberg F, et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles. 2014;3:26913.
  • Ohshima K, Inoue K, Fujiwara A, et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One. 2010;5:e13247.
  • Hannafon BN, Carpenter KJ, Berry WL, et al. Exosome-mediated microRNA signaling from breast cancer cells is altered by the anti-angiogenesis agent docosahexaenoic acid (DHA). Mol Cancer. 2015;14:133.
  • Zhang J, Li S, Li L, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics. 2015;13:17–24.
  • Hortin GL, Sviridov D, Anderson NL. High-abundance polypeptides of the human plasma proteome comprising the top 4 logs of polypeptide abundance. Clin Chem. 2008;54:1608–1616.
  • Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–579.
  • Badimon L, Suades R, Fuentes E, et al. Role of platelet-derived microvesicles as crosstalk mediators in atherothrombosis and future pharmacology targets: a link between inflammation, atherosclerosis, and thrombosis. Front Pharmacol. 2016;7:293.
  • Ge R, Tan E, Sharghi-Namini S, et al. Exosomes in cancer microenvironment and beyond: have we overlooked these extracellular messengers? Cancer Microenviron. 2012;5:323–332.
  • Buschow SI, van Balkom BW, Aalberts M, et al. MHC class II-associated proteins in B-cell exosomes and potential functional implications for exosome biogenesis. Immunol Cell Biol. 2010;88:851–856.
  • Keerthikumar S, Chisanga D, Ariyaratne D, et al. ExoCarta:a web-based compendium of exosomal cargo. J Mol Biol. 2016;428:688–692.
  • van Balkom BW, Eisele AS, Pegtel DM, et al. Quantitative and qualitative analysis of small RNAs in human endothelial cells and exosomes provides insights into localized RNA processing, degradation and sorting. J Extracell Vesicles. 2015;4:26760.
  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200:373–383.
  • Hewson C, Capraro D, Burdach J, et al. Extracellular vesicle associated long non-coding RNAs functionally enhance cell viability. Noncoding RNA Res. 2016;1:3–11.
  • Khurana R, Ranches G, Schafferer S, et al. Identification of urinary exosomal noncoding RNAs as novel biomarkers in chronic kidney disease. Rna. 2017;23:142–152.
  • Shore S, Henderson JM, Lebedev A, et al. Small RNA library preparation method for next-generation sequencing using chemical modifications to prevent adapter dimer formation. PLoS One. 2016;11:e0167009.
  • Venkatesh T, Suresh PS, Tsutsumi R. tRFs: miRNAs in disguise. Gene. 2016;579:133–138.
  • Hizir Z, Bottini S, Grandjean V, et al. RNY (YRNA)-derived small RNAs regulate cell death and inflammation in monocytes/macrophages. Cell Death Dis. 2017;8:e2530.
  • Ung TH, Madsen HJ, Hellwinkel JE, et al. Exosome proteomics reveals transcriptional regulator proteins with potential to mediate downstream pathways. Cancer Sci. 2014;105:1384–1392.
  • Liang H, Gong F, Zhang S, et al. The origin, function, and diagnostic potential of extracellular microRNAs in human body fluids. Wiley Interdiscip Rev RNA. 2014;5:285–300.
  • Huang X, Yuan T, Tschannen M, et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics. 2013;14:319.
  • Sugiura A, McLelland GL, Fon EA, et al. A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J. 2014;33:2142–2156.
  • Holliday DL, Speirs V. Choosing the right cell line for breast cancer research. Breast Cancer Res. 2011;13:215.
  • Soule HD, Vazguez J, Long A, et al. A human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst. 1973;51:1409–1416.
  • Brinkley BR, Beall PT, Wible LJ, et al. Variations in cell form and cytoskeleton in human breast carcinoma cells in vitro. Cancer Res. 1980;40:3118–3129.
  • Cailleau R, Olive M, Cruciger QV. Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro. 1978;14:911–915.
  • Keydar I, Chen L, Karby S, et al. Establishment and characterization of a cell line of human breast carcinoma origin. Eur J Cancer. 1979;15:659–670.
  • Fantozzi A, Christofori G. Mouse models of breast cancer metastasis. Breast Cancer Res. 2006;8:212.
  • Uhlen M, Fagerberg L, Hallstrom BM, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347:1260419.
  • Uhlen M, Oksvold P, Fagerberg L, et al. Towards a knowledge-based Human Protein Atlas. Nat Biotechnol. 2010;28:1248–1250.
  • Uhlen M, Bjorling E, Agaton C, et al. A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics. 2005;4:1920–1932.
  • Oliveira NC, Gomig TH, Milioli HH, et al. Comparative proteomic analysis of ductal and lobular invasive breast carcinoma. Genet Mol Res. 2016;15(2): gmr.15027701.
  • Li Y, Rong G, Kang H. Taxotere-induced elevated expression of IL8 in carcinoma-associated fibroblasts of breast invasive ductal cancer. Oncol Lett. 2017;13:1856–1860.
  • Liu YL, Zhang HM, Pan HM, et al. The relationship between apolipoprotein E gene epsilon2/epsilon3/epsilon4 polymorphism and breast cancer risk: a systematic review and meta-analysis. Onco Targets Ther. 2016;9:1241–1249.
  • Stevens KN, Wang X, Fredericksen Z, et al. Evaluation of associations between common variation in mitotic regulatory pathways and risk of overall and high grade breast cancer. Breast Cancer Res Treat. 2011;129:617–622.
  • Lucci MA, Orlandi R, Triulzi T, et al. Expression profile of tyrosine phosphatases in HER2 breast cancer cells and tumors. Cell Oncol. 2010;32:361–372.
  • Russo J, Russo IH. Molecular basis of pregnancy-induced breast cancer prevention. Horm Mol Biol Clin Investig. 2012;9:3–10.
  • Chu X, Guo X, Jiang Y, et al. Genotranscriptomic meta-analysis of the CHD family chromatin remodelers in human cancers - initial evidence of an oncogenic role for CHD7. Mol Oncol. 2017;11:1348–1360.
  • Faraji F, Hu Y, Wu G, et al. An integrated systems genetics screen reveals the transcriptional structure of inherited predisposition to metastatic disease. Genome Res. 2014;24:227–240.
  • Gonzalez-Conchas GA, Rodriguez-Romo L, Hernandez-Barajas D, et al. Epidermal growth factor receptor overexpression and outcomes in early breast cancer: a systematic review and a meta-analysis. Cancer Treat Rev. 2017;62:1–8.
  • Qian W, Tao L, Wang Y, et al. Downregulation of integrins in cancer cells and anti-platelet properties are involved in holothurian glycosaminoglycan-mediated disruption of the interaction of cancer cells and platelets in hematogenous metastasis. J Vasc Res. 2015;52:197–209.
  • Chi Y, Huang S, Wang L, et al. CDK11p58 inhibits ERalpha-positive breast cancer invasion by targeting integrin beta3 via the repression of ERalpha signaling. BMC Cancer. 2014;14:577.
  • Gong Y, He T, Yang L, et al. The role of miR-100 in regulating apoptosis of breast cancer cells. Sci Rep. 2015;5:11650.
  • Marcotte R, Sayad A, Brown KR, et al. Functional genomic landscape of human breast cancer drivers, vulnerabilities, and resistance. Cell. 2016;164:293–309.
  • Abdelkarim M, Vintonenko N, Starzec A, et al. Invading basement membrane matrix is sufficient for MDA-MB-231 breast cancer cells to develop a stable in vivo metastatic phenotype. PLoS One. 2011;6:e23334.
  • Cine N, Baykal AT, Sunnetci D, et al. Identification of ApoA1, HPX and POTEE genes by omic analysis in breast cancer. Oncol Rep. 2014;32:1078–1086.
  • Qian L, Gao X, Huang H, et al. PRSS3 is a prognostic marker in invasive ductal carcinoma of the breast. Oncotarget. 2017;8:21444–21453.
  • Ma R, Ye X, Cheng H, et al. PRSS3 expression is associated with tumor progression and poor prognosis in epithelial ovarian cancer. Gynecol Oncol. 2015;137:546–552.
  • Hockla A, Radisky DC, Radisky ES. Mesotrypsin promotes malignant growth of breast cancer cells through shedding of CD109. Breast Cancer Res Treat. 2010;124:27–38.
  • Yang L, Shi T, Liu F, et al. REV3L, a promising target in regulating the chemosensitivity of cervical cancer cells. PLoS One. 2015;10:e0120334.
  • Varadi V, Bevier M, Grzybowska E, et al. Genetic variation in genes encoding for polymerase zeta subunits associates with breast cancer risk, tumour characteristics and survival. Breast Cancer Res Treat. 2011;129:235–245.
  • Roger S, Gillet L, Le Guennec JY, et al. Voltage-gated sodium channels and cancer: is excitability their primary role? Front Pharmacol. 2015;6:152.
  • Gau DM, Lesnock JL, Hood BL, et al. BRCA1 deficiency in ovarian cancer is associated with alteration in expression of several key regulators of cell motility - A proteomics study. Cell Cycle. 2015;14:1884–1892.
  • Gur-Dedeoglu B, Konu O, Kir S, et al. A resampling-based meta-analysis for detection of differential gene expression in breast cancer. BMC Cancer. 2008;8:396.
  • Song J, Yang W, Shih IM, et al. Identification of BCOX1, a novel gene overexpressed in breast cancer. Biochim Biophys Acta. 2006;1760:62–69.
  • Schuetz CS, Bonin M, Clare SE, et al. Progression-specific genes identified by expression profiling of matched ductal carcinomas in situ and invasive breast tumors, combining laser capture microdissection and oligonucleotide microarray analysis. Cancer Res. 2006;66:5278–5286.
  • Lee S, Stewart S, Nagtegaal I, et al. Differentially expressed genes regulating the progression of ductal carcinoma in situ to invasive breast cancer. Cancer Res. 2012;72:4574–4586.
  • Michael M, Begum R, Fong K, et al. BPAG1-e restricts keratinocyte migration through control of adhesion stability. J Invest Dermatol. 2014;134:773–782.
  • Kuchnio A, Dewerchin M, Carmeliet P. The PHD2 oxygen sensor paves the way to metastasis. Oncotarget. 2015;6:35149–35150.
  • Bordoli MR, Stiehl DP, Borsig L, et al. Prolyl-4-hydroxylase PHD2- and hypoxia-inducible factor 2-dependent regulation of amphiregulin contributes to breast tumorigenesis. Oncogene. 2011;30:548–560.
  • Singh M, Devi U, Roy S, et al. Prolyl hydroxylase mediated inhibition of fatty acid synthase to combat tumor growth in mammary gland carcinoma. Breast Cancer. 2016;23:820–829.
  • Paolicchi E, Crea F, Farrar WL, et al. Histone lysine demethylases in breast cancer. Crit Rev Oncol Hematol. 2013;86:97–103.
  • Hou J, Wu J, Dombkowski A, et al. Genomic amplification and a role in drug-resistance for the KDM5A histone demethylase in breast cancer. Am J Transl Res. 2012;4:247–256.
  • Gale M, Sayegh J, Cao J, et al. Screen-identified selective inhibitor of lysine demethylase 5A blocks cancer cell growth and drug resistance. Oncotarget. 2016;7:39931–39944.
  • Newbold RF, Mokbel K. Evidence for a tumour suppressor function of SETD2 in human breast cancer: a new hypothesis. Anticancer Res. 2010;30:3309–3311.
  • Al Sarakbi W, Sasi W, Jiang WG, et al. The mRNA expression of SETD2 in human breast cancer: correlation with clinico-pathological parameters. BMC Cancer. 2009;9:290.
  • Shen H, Li L, Zhou S, et al. The role of ADAM17 in tumorigenesis and progression of breast cancer. Tumour Biol. 2016;37(12):15359–15370.
  • Narita D, Seclaman E, Ilina R, et al. ADAM12 and ADAM17 gene expression in laser-capture microdissected and non-microdissected breast tumors. Pathol Oncol Res. 2011;17:375–385.
  • Zheng X, Jiang F, Katakowski M, et al. ADAM17 promotes breast cancer cell malignant phenotype through EGFR-PI3K-AKT activation. Cancer Biol Ther. 2009;8:1045–1054.
  • Wang CY, Lai MD, Phan NN, et al. Meta-analysis of public microarray datasets reveals voltage-gated calcium gene signatures in clinical cancer patients. PLoS One. 2015;10:e0125766.
  • Yamaga R, Ikeda K, Horie-Inoue K, et al. RNA sequencing of MCF-7 breast cancer cells identifies novel estrogen-responsive genes with functional estrogen receptor-binding sites in the vicinity of their transcription start sites. Horm Cancer. 2013;4:222–232.
  • Bjorklund SS, Panda A, Kumar S, et al. Widespread alternative exon usage in clinically distinct subtypes of Invasive Ductal Carcinoma. Sci Rep. 2017;7:5568.
  • Wang H, Wang B, Zhu W, et al. Lentivirus-mediated knockdown of myosin VI inhibits cell proliferation of breast cancer cell. Cancer Biother Radiopharm. 2015;30:330–335.
  • De Marchi T, Timmermans AM, Smid M, et al. Annexin-A1 and caldesmon are associated with resistance to tamoxifen in estrogen receptor positive recurrent breast cancer. Oncotarget. 2016;7:3098–3110.
  • Zou JX, Duan Z, Wang J, et al. Kinesin family deregulation coordinated by bromodomain protein ANCCA and histone methyltransferase MLL for breast cancer cell growth, survival, and tamoxifen resistance. Mol Cancer Res. 2014;12:539–549.
  • Yuasa-Kawada J, Kinoshita-Kawada M, Rao Y, et al. Deubiquitinating enzyme USP33/VDU1 is required for Slit signaling in inhibiting breast cancer cell migration. Proc Natl Acad Sci U S A. 2009;106:14530–14535.
  • Chen NP, Uddin B, Voit R, et al. Human phosphatase CDC14A is recruited to the cell leading edge to regulate cell migration and adhesion. Proc Natl Acad Sci U S A. 2016;113:990–995.
  • Sohn EJ, Jung DB, Lee H, et al. CNOT2 promotes proliferation and angiogenesis via VEGF signaling in MDA-MB-231 breast cancer cells. Cancer Lett. 2017;412:88–98.
  • Li W, Liu C, Zhao C, et al. Downregulation of beta3 integrin by miR-30a-5p modulates cell adhesion and invasion by interrupting Erk/Ets1 network in triple-negative breast cancer. Int J Oncol. 2016;48:1155–1164.
  • Carter RZ, Micocci KC, Natoli A, et al. Tumour but not stromal expression of beta3 integrin is essential, and is required early, for spontaneous dissemination of bone-metastatic breast cancer. J Pathol. 2015;235:760–772.
  • Liu T, Zhang XY, He XH, et al. High levels of BCOX1 expression are associated with poor prognosis in patients with invasive ductal carcinomas of the breast. PLoS One. 2014;9:e86952.