Identifying high-grade serous ovarian carcinoma–specific extracellular vesicles by polyketone-coated nanowires

Cancer cell–derived extracellular vesicles (EVs) have unique protein profiles, making them promising targets as disease biomarkers. High-grade serous ovarian carcinoma (HGSOC) is the deadly subtype of epithelial ovarian cancer, and we aimed to identify HGSOC-specific membrane proteins. Small EVs (sEVs) and medium/large EVs (m/lEVs) from cell lines or patient serum and ascites were analyzed by LC-MS/MS, revealing that both EV subtypes had unique proteomic characteristics. Multivalidation steps identified FRα, Claudin-3, and TACSTD2 as HGSOC-specific sEV proteins, but m/lEV-associated candidates were not identified. In addition, for using a simple-to-use microfluidic device for EV isolation, polyketone-coated nanowires (pNWs) were developed, which efficiently purify sEVs from biofluids. Multiplexed array assays of sEVs isolated by pNW showed specific detectability in cancer patients and predicted clinical status. In summary, the HGSOC-specific marker detection by pNW are a promising platform as clinical biomarkers, and these insights provide detailed proteomic aspects of diverse EVs in HGSOC patients.

[1]  Y. Hijikata,et al.  Alkali metal ion binding using cyclic polyketones. , 2022, Chemical communications.

[2]  T. Ochiya,et al.  Molecular profiling of extracellular vesicles via charge-based capture using oxide nanowire microfluidics. , 2021, Biosensors & bioelectronics.

[3]  Y. Baba,et al.  Annealed ZnO/Al2O3 Core-Shell Nanowire as a Platform to Capture RNA in Blood Plasma , 2021, Nanomaterials.

[4]  M. Parmar,et al.  Ovarian cancer population screening and mortality after long-term follow-up in the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS): a randomised controlled trial , 2021, The Lancet.

[5]  Y. Baba,et al.  Urinary MicroRNA-Based Diagnostic Model for Central Nervous System Tumors Using Nanowire Scaffolds. , 2021, ACS applied materials & interfaces.

[6]  T. Ochiya,et al.  Exosomes and extracellular vesicles: Rethinking the essential values in cancer biology. , 2021, Seminars in cancer biology.

[7]  Y. Baba,et al.  Ammonia-Induced Seed Layer Transformations in a Hydrothermal Growth Process of Zinc Oxide Nanowires , 2020 .

[8]  A. Ivanov,et al.  Technologies and Standardization in Research on Extracellular Vesicles , 2020, Trends in Biotechnology.

[9]  N. Shioya,et al.  MAIRS: Innovation of Molecular Orientation Analysis in a Thin Film , 2020 .

[10]  U. Banerji,et al.  Exploiting the folate receptor α in oncology , 2020, Nature Reviews Clinical Oncology.

[11]  A. Jemal,et al.  Cancer statistics, 2020 , 2020, CA: a cancer journal for clinicians.

[12]  Romaric Lacroix,et al.  MIFlowCyt-EV: a framework for standardized reporting of extracellular vesicle flow cytometry experiments , 2020, Journal of extracellular vesicles.

[13]  L. Laurent,et al.  Mechanisms of nuclear content loading to exosomes , 2019, Science Advances.

[14]  T. Whiteside,et al.  Challenges in Exosome Isolation and Analysis in Health and Disease , 2019, International journal of molecular sciences.

[15]  Michael A. Freitas,et al.  A microfluidic chip enables isolation of exosomes and establishment of their protein profiles and associated signaling pathways in ovarian cancer. , 2019, Cancer research.

[16]  Yumehiro Manabe,et al.  Two-Step Transformation of Aliphatic Polyketones into π-Conjugated Polyimines. , 2019, The Journal of organic chemistry.

[17]  Wei Zhang,et al.  Proteomics profiling of plasma exosomes in epithelial ovarian cancer: A potential role in the coagulation cascade, diagnosis and prognosis , 2019, International journal of oncology.

[18]  A. Godwin,et al.  Ultrasensitive detection of circulating exosomes with a 3D-nanopatterned microfluidic chip , 2019, Nature Biomedical Engineering.

[19]  Jing Xu,et al.  Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines , 2018, Journal of Extracellular Vesicles.

[20]  T. Ochiya,et al.  Integrated extracellular microRNA profiling for ovarian cancer screening , 2018, Nature Communications.

[21]  David W. Greening,et al.  Extracellular vesicles in cancer — implications for future improvements in cancer care , 2018, Nature Reviews Clinical Oncology.

[22]  Tushar Patel,et al.  Circulating Extracellular Vesicles in Human Disease. , 2018, The New England journal of medicine.

[23]  N. Girard,et al.  Clinical potential of circulating tumour DNA in patients receiving anticancer immunotherapy , 2018, Nature Reviews Clinical Oncology.

[24]  Yu Saito,et al.  Oligoacetylacetones as shapable carbon chains and their transformation to oligoimines for construction of metal-organic architectures , 2018, Communications Chemistry.

[25]  Graça Raposo,et al.  Shedding light on the cell biology of extracellular vesicles , 2018, Nature Reviews Molecular Cell Biology.

[26]  T. Ochiya,et al.  Unveiling massive numbers of cancer-related urinary-microRNA candidates via nanowires , 2017, Science Advances.

[27]  S. Jordan,et al.  Epidemiology of epithelial ovarian cancer. , 2017, Best practice & research. Clinical obstetrics & gynaecology.

[28]  T. Ochiya,et al.  Malignant extracellular vesicles carrying MMP1 mRNA facilitate peritoneal dissemination in ovarian cancer , 2017, Nature Communications.

[29]  C. Théry,et al.  Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes , 2016, Proceedings of the National Academy of Sciences.

[30]  M Kersaudy-Kerhoas,et al.  Exosome isolation: a microfluidic road-map. , 2015, Lab on a chip.

[31]  C. Théry,et al.  Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. , 2014, Annual review of cell and developmental biology.

[32]  Hakho Lee,et al.  Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor , 2014, Nature Biotechnology.

[33]  Yusuke Yoshioka,et al.  Ultra-sensitive liquid biopsy of circulating extracellular vesicles using ExoScreen , 2014, Nature Communications.

[34]  M. Ratajczak,et al.  Exosomes: an overview of biogenesis, composition and role in ovarian cancer , 2014, Journal of Ovarian Research.

[35]  J. Vandesompele,et al.  The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling , 2014, Journal of extracellular vesicles.

[36]  C. Sander,et al.  Evaluating cell lines as tumour models by comparison of genomic profiles , 2013, Nature Communications.

[37]  B. Monk,et al.  Latest research and treatment of advanced-stage epithelial ovarian cancer , 2013, Nature Reviews Clinical Oncology.

[38]  She Chen,et al.  Characterization and proteomic analysis of ovarian cancer-derived exosomes. , 2013, Journal of proteomics.

[39]  S. Kaye,et al.  Meeting the challenge of ascites in ovarian cancer: new avenues for therapy and research , 2013, Nature Reviews Cancer.

[40]  Lynne T. Bemis,et al.  Standardization of sample collection, isolation and analysis methods in extracellular vesicle research , 2013, Journal of extracellular vesicles.

[41]  P. Chang,et al.  Comparative and targeted proteomic analyses of urinary microparticles from bladder cancer and hernia patients. , 2012, Journal of proteome research.

[42]  Fujio Izumi,et al.  VESTA 3 for three-dimensional visualization of crystal, volumetric and morphology data , 2011 .

[43]  Kenneth P. Nephew,et al.  Rethinking ovarian cancer: recommendations for improving outcomes , 2011, Nature Reviews Cancer.

[44]  Benjamin J. Raphael,et al.  Integrated Genomic Analyses of Ovarian Carcinoma , 2011, Nature.

[45]  F. Magni,et al.  Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery , 2011, Proteomics.

[46]  M. Rots,et al.  EpCAM in carcinogenesis: the good, the bad or the ugly. , 2010, Carcinogenesis.

[47]  R. Roden,et al.  Claudin-containing exosomes in the peripheral circulation of women with ovarian cancer , 2009, BMC Cancer.

[48]  J. Geddes,et al.  What is a randomised controlled trial? , 2009, Epidemiologia e Psichiatria Sociale.

[49]  Y. Tatsumi,et al.  Redundant and differential regulation of multiple licensing factors ensures prevention of re-replication in normal human cells , 2009, Journal of Cell Science.

[50]  M. Fujita,et al.  Oncogenic transformation of human ovarian surface epithelial cells with defined cellular oncogenes. , 2009, Carcinogenesis.

[51]  S. Hirohashi,et al.  An in vitro multistep carcinogenesis model for human cervical cancer. , 2008, Cancer research.

[52]  T. Hasegawa Advanced multiple-angle incidence resolution spectrometry for thin-layer analysis on a low-refractive-index substrate. , 2007, Analytical chemistry.

[53]  J. Garber,et al.  A candidate precursor to serous carcinoma that originates in the distal fallopian tube , 2007 .

[54]  T. Hasegawa A Novel Measurement Technique of Pure Out-of-Plane Vibrational Modes in Thin Films on a Nonmetallic Material with No Polarizer , 2002 .

[55]  P. V. van Diest,et al.  Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer , 2001, The Journal of pathology.

[56]  Kresse,et al.  Efficient iterative schemes for ab initio total-energy calculations using a plane-wave basis set. , 1996, Physical review. B, Condensed matter.

[57]  I Aitken,et al.  Swearing: The Good, the Bad & the Ugly. , 2017 .

[58]  Alessandro Lugli,et al.  Frequent EpCam protein expression in human carcinomas. , 2004, Human pathology.