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Biological Chemistry

Editor-in-Chief: Brüne, Bernhard

Editorial Board: Buchner, Johannes / Lei, Ming / Ludwig, Stephan / Sies, Helmut / Thomas, Douglas D. / Turk, Boris / Wittinghofer, Alfred

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Volume 394, Issue 10


Current methods for the isolation of extracellular vesicles

Fatemeh Momen-Heravi
  • Laboratory for Innovative Translational Technologies, Harvard Medical School, 77 Louis Pasteur Avenue, Harvard Medical School, Boston, MA 02115, USA
  • These authors contributed equally to this work.
  • Other articles by this author:
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/ Leonora Balaj
  • Laboratory for Innovative Translational Technologies, Harvard Medical School, 77 Louis Pasteur Avenue, Harvard Medical School, Boston, MA 02115, USA
  • Department of Neurology and Radiology, Massachusetts General Hospital, 149 13th Street, Charlestown, MA 02129, USA
  • These authors contributed equally to this work.
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/ Sara Alian / Pierre-Yves Mantel
  • Department of Immunology and Infectious Diseases, Harvard School of Public Health, 665 Huntington Avenue, Boston, MA 02120, USA
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/ Allison E. Halleck
  • Laboratory for Innovative Translational Technologies, Harvard Medical School, 77 Louis Pasteur Avenue, Harvard Medical School, Boston, MA 02115, USA
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/ Alexander J. Trachtenberg
  • Laboratory for Innovative Translational Technologies, Harvard Medical School, 77 Louis Pasteur Avenue, Harvard Medical School, Boston, MA 02115, USA
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/ Cesar E. Soria / Shanice Oquin / Christina M. Bonebreak / Elif Saracoglu
  • Faculty of Dentistry, Istanbul University, Turgut Özal Caddesi (Millet Cd.), 34390 Istanbul, Turkey
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/ Johan Skog / Winston Patrick Kuo
  • Corresponding author
  • Laboratory for Innovative Translational Technologies, Harvard Medical School, 77 Louis Pasteur Avenue, Harvard Medical School, Boston, MA 02115, USA
  • Department of Developmental Biology, Harvard School of Dental Medicine, Boston, MA 02115, USA
  • Email
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Published Online: 2013-06-14 | DOI: https://doi.org/10.1515/hsz-2013-0141


Extracellular vesicles (EVs), including microvesicles and exosomes, are nano- to micron-sized vesicles, which may deliver bioactive cargos that include lipids, growth factors and their receptors, proteases, signaling molecules, as well as mRNA and non-coding RNA, released from the cell of origin, to target cells. EVs are released by all cell types and likely induced by mechanisms involved in oncogenic transformation, environmental stimulation, cellular activation, oxidative stress, or death. Ongoing studies investigate the molecular mechanisms and mediators of EVs-based intercellular communication at physiological and oncogenic conditions with the hope of using this information as a possible source for explaining physiological processes in addition to using them as therapeutic targets and disease biomarkers in a variety of diseases. A major limitation in this evolving discipline is the hardship and the lack of standardization for already challenging techniques to isolate EVs. Technical advances have been accomplished in the field of isolation with improving knowledge and emerging novel technologies, including ultracentrifugation, microfluidics, magnetic beads and filtration-based isolation methods. In this review, we will discuss the latest advances in methods of isolation methods and production of clinical grade EVs as well as their advantages and disadvantages, and the justification for their support and the challenges that they encounter.

Keywords: clinical grade EVs; exosomes; magnetic beads; microvesicles; sedimentation efficiency; ultracentrifugation


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About the article

Corresponding author: Winston Patrick Kuo, Harvard Catalyst Laboratory for Innovative Translational Technologies, Harvard Medical School, Boston, MA 02115, USA; and Department of Developmental Biology, Harvard School of Dental Medicine, Boston, MA 02115, USA

Received: 2013-02-23

Accepted: 2013-06-13

Published Online: 2013-06-14

Published in Print: 2013-10-01

Citation Information: Biological Chemistry, Volume 394, Issue 10, Pages 1253–1262, ISSN (Online) 1437-4315, ISSN (Print) 1431-6730, DOI: https://doi.org/10.1515/hsz-2013-0141.

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Biomedicines, 2018, Volume 6, Number 3, Page 79
Shuang Cai, Bin Luo, Peipei Jiang, Xiaoxi Zhou, Fang Lan, Qiangying Yi, and Yao Wu
Nanoscale, 2018
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Stem Cell Research & Therapy, 2018, Volume 9, Number 1
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Micromachines, 2018, Volume 9, Number 6, Page 306
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Transfusion Medicine and Hemotherapy, 2018, Volume 45, Number 3, Page 185
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PROTEOMICS - Clinical Applications, 2018, Page 1700142
Diego de Souza Gonçalves, Marina da Silva Ferreira, Susie Coutinho Liedke, Kamilla Xavier Gomes, Gabriel Afonso de Oliveira, Pedro Ernesto Lopes Leão, Gabriele Vargas Cesar, Sergio H. Seabra, Juliana Reis Cortines, Arturo Casadevall, Leonardo Nimrichter, Gilberto Barbosa Domont, Magno Rodrigues Junqueira, Jose Mauro Peralta, and Allan J. Guimaraes
Virulence, 2018, Volume 9, Number 1, Page 818
Raquel Bello-Morales, Beatriz Praena, Carmen de la Nuez, María Teresa Rejas, Milagros Guerra, Marcos Galán-Ganga, Manuel Izquierdo, Víctor Calvo, Claude Krummenacher, José Antonio López-Guerrero, and Richard M. Longnecker
Journal of Virology, 2018, Volume 92, Number 10, Page e00088-18
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Matjaž Stenovec, Eva Lasič, Pia Pužar Dominkuš, Saša Trkov Bobnar, Robert Zorec, Metka Lenassi, and Marko Kreft
Molecular Neurobiology, 2018
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Analytical and Bioanalytical Chemistry, 2018
Nicole Osier, Vida Motamedi, Katie Edwards, Ava Puccio, Ramon Diaz-Arrastia, Kimbra Kenney, and Jessica Gill
Molecular Neurobiology, 2018
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Journal of Leukocyte Biology, 2018
Young-Eun Cho, Byoung-Joon Song, Mohammed Akbar, and Moon-Chang Baek
Pharmacology & Therapeutics, 2018
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Sarah E Thacker, Manisha Nautiyal, Monicah A Otieno, Paul B Watkins, and Merrie Mosedale
Toxicological Sciences, 2018
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Journal of Extracellular Vesicles, 2018, Volume 7, Number 1, Page 1440131
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Frontiers in Immunology, 2018, Volume 9
Gebeyaw Getnet Mekonnen, Mark Pearson, Alex Loukas, and Javier Sotillo
Expert Review of Vaccines, 2018, Page 1
Maria Yu. Konoshenko, Evgeniy A. Lekchnov, Alexander V. Vlassov, and Pavel P. Laktionov
BioMed Research International, 2018, Volume 2018, Page 1
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Molecular Therapy - Nucleic Acids, 2018, Volume 10, Page 131
Marcel I. Ramirez, Maria G. Amorim, Catarina Gadelha, Ivana Milic, Joshua A. Welsh, Vanessa M. Freitas, Muhammad Nawaz, Naveed Akbar, Yvonne Couch, Laura Makin, Fiona Cooke, Andre L. Vettore, Patricia X. Batista, Roberta Freezor, Julia A. Pezuk, Lívia Rosa-Fernandes, Ana Claudia O. Carreira, Andrew Devitt, Laura Jacobs, Israel T. Silva, Gillian Coakley, Diana N. Nunes, Dave Carter, Giuseppe Palmisano, and Emmanuel Dias-Neto
Nanoscale, 2018
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Analytica Chimica Acta, 2017
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Biomaterials Science, 2018
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Artificial Cells, Nanomedicine, and Biotechnology, 2017, Page 1
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Analytical Chemistry, 2017
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Journal of Circulating Biomarkers, 2014, Volume 3, Page 3
Kanchan Vaswani, Yong Qin Koh, Fatema B. Almughlliq, Hassendrini N. Peiris, and Murray D. Mitchell
Reproductive Biology, 2017
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PLOS ONE, 2017, Volume 12, Number 10, Page e0186534
Jie Wang, Wei Li, Zhichao Lu, Leicheng Zhang, Yu Hu, Qiubai Li, Wei Du, Xiaojun Feng, Haibo Jia, and Bi-Feng Liu
Nanoscale, 2017
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Frontiers in Cardiovascular Medicine, 2017, Volume 4
Xuan Gao, Carlos Salomon, and Dilys J. Freeman
Frontiers in Endocrinology, 2017, Volume 8
Stinne R. Greisen, Yan Yan, Aida S. Hansen, Morten T. Venø, Jens R. Nyengaard, Søren K. Moestrup, Malene Hvid, Gordon J. Freeman, Jørgen Kjems, and Bent Deleuran
Frontiers in Immunology, 2017, Volume 8
Jeffrey D. McBride, Luis Rodriguez-Menocal, Wellington Guzman, Ambar Candanedo, Marta Garcia-Contreras, and Evangelos V. Badiavas
Stem Cells and Development, 2017
Banishree Saha, Fatemeh Momen-Heravi, Karen Kodys, and Gyongyi Szabo
Journal of Biological Chemistry, 2016, Volume 291, Number 1, Page 149
Gyongyi Szabo and Fatemeh Momen-Heravi
Nature Reviews Gastroenterology & Hepatology, 2017
Davide Zabeo, Aleksander Cvjetkovic, Cecilia Lässer, Martin Schorb, Jan Lötvall, and Johanna L Höög
Journal of Extracellular Vesicles, 2017, Volume 6, Number 1, Page 1329476
Elham Behzadi, Hamideh Mahmoodzadeh Hosseini, and Abbas Ali Imani Fooladi
Microbial Pathogenesis, 2017, Volume 110, Page 1
Juhi Sharma, Jeffrey M. Hampton, Giancarlo R. Valiente, Takuma Wada, Holly Steigelman, Matthew C. Young, Rachel R. Spurbeck, Alisa D. Blazek, Steffi Bösh, Wael N. Jarjour, and Nicholas A. Young
Frontiers in Immunology, 2017, Volume 8
Carina Hromada, Severin Mühleder, Johannes Grillari, Heinz Redl, and Wolfgang Holnthoner
Frontiers in Physiology, 2017, Volume 8
Sahil Inamdar, Rajeshwar Nitiyanandan, and Kaushal Rege
Bioengineering & Translational Medicine, 2017, Volume 2, Number 1, Page 70
Shimeng Fang, Hongzhu Tian, Xiancheng Li, Dong Jin, Xiaojie Li, Jing Kong, Chun Yang, Xuesong Yang, Yao Lu, Yong Luo, Bingcheng Lin, Weidong Niu, Tingjiao Liu, and Aamir Ahmad
PLOS ONE, 2017, Volume 12, Number 4, Page e0175050
Irene Vanni, Angela Alama, Francesco Grossi, Maria Giovanna Dal Bello, and Simona Coco
Drug Discovery Today, 2017, Volume 22, Number 6, Page 927
Ruqayyah J. Almizraq, Jerard Seghatchian, Jelena L. Holovati, and Jason P. Acker
Transfusion and Apheresis Science, 2017, Volume 56, Number 2, Page 254
Hyejin Kang, Jiyoon Kim, and Jaesung Park
Micro and Nano Systems Letters, 2017, Volume 5, Number 1
Parissa Ziaei, Jonathan J. Geruntho, Oscar G. Marin-Flores, Clifford E. Berkman, and M. Grant Norton
Journal of Materials Science, 2017, Volume 52, Number 12, Page 6907
Fang Yang, Xiangzhi Liao, Yuan Tian, and Guiying Li
Biotechnology Journal, 2017, Volume 12, Number 4, Page 1600699
Aleksander Cvjetkovic, Jan Lötvall, and Cecilia Lässer
Journal of Extracellular Vesicles, 2014, Volume 3, Number 1, Page 23111
William E. Butler, Nadia Atai, Bob Carter, and Fred Hochberg
Journal of Extracellular Vesicles, 2014, Volume 3, Number 1, Page 24247
Shima Gholizadeh, Mohamed Shehata Draz, Maryam Zarghooni, Amir Sanati-Nezhad, Saeid Ghavami, Hadi Shafiee, and Mohsen Akbari
Biosensors and Bioelectronics, 2017, Volume 91, Page 588
Olivia Twu, Patricia J. Johnson, and Laura J. Knoll
PLoS Pathogens, 2014, Volume 10, Number 8, Page e1004289
Daniel Enderle, Alexandra Spiel, Christine M. Coticchia, Emily Berghoff, Romy Mueller, Martin Schlumpberger, Markus Sprenger-Haussels, Jonathan M. Shaffer, Eric Lader, Johan Skog, Mikkel Noerholm, and Gerrit J. Bouma
PLOS ONE, 2015, Volume 10, Number 8, Page e0136133
David W. Greening, Rong Xu, Shashi K. Gopal, Alin Rai, and Richard J. Simpson
Expert Review of Proteomics, 2017, Volume 14, Number 1, Page 69
Giuliana Di Rocco, Silvia Baldari, and Gabriele Toietta
Stem Cells International, 2016, Volume 2016, Page 1
Dionne Tannetta, Gavin Collett, Manu Vatish, Chris Redman, and Ian Sargent
Placenta, 2017, Volume 52, Page 134
Monica Reis, Justyna Ogonek, Marsela Qesari, Nuno M. Borges, Lindsay Nicholson, Liane Preußner, Anne Mary Dickinson, Xiao-nong Wang, Eva M. Weissinger, and Anne Richter
Frontiers in Immunology, 2016, Volume 7
Golam Kibria, Erika K. Ramos, Katelyn E. Lee, Sarah Bedoyan, Simo Huang, Ravand Samaeekia, Jaffre J. Athman, Clifford V. Harding, Jan Lötvall, Lyndsay Harris, Cheryl L. Thompson, and Huiping Liu
Scientific Reports, 2016, Volume 6, Number 1
Boon Siew Chia, Yen Peng Low, Qing Wang, Pin Li, and Zhiqiang Gao
TrAC Trends in Analytical Chemistry, 2017, Volume 86, Page 93
Isabel Huang-Doran, Chen-Yu Zhang, and Antonio Vidal-Puig
Trends in Endocrinology & Metabolism, 2017, Volume 28, Number 1, Page 3
Ruqayyah J. Almizraq, Jerard Seghatchian, and Jason P. Acker
Transfusion and Apheresis Science, 2016, Volume 55, Number 3, Page 281
Roman Štukelj, Karin Schara, Apolonija Bedina - Zavec, Vid Šuštar, Manca Pajnič, Ljubiša Pađen, Judita Lea Krek, Veronika Kralj-Iglič, Anita Mrvar-Brečko, and Rado Janša
European Journal of Pharmaceutical Sciences, 2017, Volume 98, Page 17
Dominique Ingato, Jong Uk Lee, Sang Jun Sim, and Young Jik Kwon
Journal of Controlled Release, 2016, Volume 241, Page 174
Dionne Tannetta, Ieva Masliukaite, Manu Vatish, Christopher Redman, and Ian Sargent
Journal of Reproductive Immunology, 2017, Volume 119, Page 98
Christopher Tricarico, James Clancy, and Crislyn D'Souza-Schorey
Small GTPases, 2016, Page 1
Che-Ming Liu, Chia-Ling Hsieh, Chia-Ning Shen, Cheng-Chieh Lin, Katsumi Shigemura, and Shian-Ying Sung
International Journal of Urology, 2016, Volume 23, Number 9, Page 734
Christian Hacker, Jalal Asadi, Christos Pliotas, Sophie Ferguson, Lee Sherry, Phedra Marius, Javier Tello, David Jackson, James Naismith, and John Milton Lucocq
Scientific Reports, 2016, Volume 6, Number 1
Sylwia Koniusz, Anna Andrzejewska, Maurizio Muraca, Amit K. Srivastava, Miroslaw Janowski, and Barbara Lukomska
Frontiers in Cellular Neuroscience, 2016, Volume 10
Hui Ye and Austen Curcuru
Medical & Biological Engineering & Computing, 2016, Volume 54, Number 12, Page 1871
Raj Kishore, Venkata Naga Srikanth Garikipati, and Anna Gumpert
Journal of Cardiovascular Translational Research, 2016, Volume 9, Number 3, Page 169
Hina Kalra, Gregor Drummen, and Suresh Mathivanan
International Journal of Molecular Sciences, 2016, Volume 17, Number 2, Page 170
Zheng Zhao, Yang Yang, Yong Zeng, and Mei He
Lab Chip, 2016, Volume 16, Number 3, Page 489
Gabriella Pocsfalvi, Christopher Stanly, Immacolata Fiume, and Károly Vékey
Journal of Chromatography A, 2016, Volume 1439, Page 26
Rachel E. Crossland, Jean Norden, Louis A. Bibby, Joanna Davis, and Anne M. Dickinson
Journal of Immunological Methods, 2016, Volume 429, Page 39
Mikhail A. Livshits, Elena Khomyakova, Evgeniy G. Evtushenko, Vassili N. Lazarev, Nikolay A. Kulemin, Svetlana E. Semina, Edward V. Generozov, and Vadim M. Govorun
Scientific Reports, 2015, Volume 5, Number 1
Juan Salazar, Luis Carlos Olivar, Eduardo Ramos, Mervin Chávez-Castillo, Joselyn Rojas, and Valmore Bermúdez
Cholesterol, 2015, Volume 2015, Page 1
Brigitte Bisaro, Giorgia Mandili, Alice Poli, Andrea Piolatto, Valentina Papa, Francesco Novelli, Giovanna Cenacchi, Marco Forni, and Cristina Zanini
Molecular and Cellular Therapies, 2015, Volume 3, Number 1
Johann Mar Gudbergsson, Kasper Bendix Johnsen, Martin Najbjerg Skov, and Meg Duroux
Cytotechnology, 2016, Volume 68, Number 4, Page 579
Konstantin Yakimchuk
Materials and Methods, 2015, Volume 5
Fatemeh Momen-Heravi, Banishree Saha, Karen Kodys, Donna Catalano, Abhishek Satishchandran, and Gyongyi Szabo
Journal of Translational Medicine, 2015, Volume 13, Number 1
Antonella D'Ambrosio, Simona Pontecorvo, Tania Colasanti, Silvia Zamboni, Ada Francia, and Paola Margutti
Autoimmunity Reviews, 2015, Volume 14, Number 12, Page 1097
Diederick Duijvesz, C. Yin L. Versluis, Christa A.M. van der Fels, Mirella S. Vredenbregt-van den Berg, Janne Leivo, Mari T. Peltola, Chris H. Bangma, Kim S.I. Pettersson, and Guido Jenster
International Journal of Cancer, 2015, Volume 137, Number 12, Page 2869
A. Liga, A. D. B. Vliegenthart, W. Oosthuyzen, J. W. Dear, and M. Kersaudy-Kerhoas
Lab Chip, 2015, Volume 15, Number 11, Page 2388
Fatemeh Momen-Heravi, Shashi Bala, Karen Kodys, and Gyongyi Szabo
Scientific Reports, 2015, Volume 5, Number 1
Heather C. Inglis, Ali Danesh, Avani Shah, Jacques Lacroix, Philip C. Spinella, and Philip J. Norris
Cytometry Part A, 2015, Volume 87, Number 11, Page 1052
Gabriella Pocsfalvi, Christopher Stanly, Annalisa Vilasi, Immacolata Fiume, Giovambattista Capasso, Lilla Turiák, Edit I Buzas, and Károly Vékey
Mass Spectrometry Reviews, 2016, Volume 35, Number 1, Page 3
Joel Z. Nordin, Yi Lee, Pieter Vader, Imre Mäger, Henrik J. Johansson, Wolf Heusermann, Oscar P.B. Wiklander, Mattias Hällbrink, Yiqi Seow, Jarred J. Bultema, Jonathan Gilthorpe, Tim Davies, Paul J. Fairchild, Susanne Gabrielsson, Nicole C. Meisner-Kober, Janne Lehtiö, C.I. Edvard Smith, Matthew J.A. Wood, and Samir EL Andaloussi
Nanomedicine: Nanotechnology, Biology and Medicine, 2015, Volume 11, Number 4, Page 879
Hui Ye and Austen Curcuru
BMC Biophysics, 2015, Volume 8, Number 1, Page 2
Luca Musante, Dorota Tataruch, Dongfeng Gu, Alberto Benito-Martin, Giulio Calzaferri, Sinead Aherne, and Harry Holthofer
Scientific Reports, 2015, Volume 4, Number 1
Hongqi Xin, Yi Li, and Michael Chopp
Frontiers in Cellular Neuroscience, 2014, Volume 8
Marcella Franquesa, Martin J. Hoogduijn, Elia Ripoll, Franka Luk, Mahdi Salih, Michiel G. H. Betjes, Juan Torras, Carla C. Baan, Josep M. Grinyó, and Ana Maria Merino
Frontiers in Immunology, 2014, Volume 5
Haitao Gu, Anne-Marie C. Overstreet, and Yongguang Yang
Nano LIFE, 2014, Volume 04, Number 04, Page 1441017
Ivana Kawikova and Philip W. Askenase
Brain Research, 2015, Volume 1617, Page 63
Kirsten Lindner, Joerg Haier, Zhe Wang, David I. Watson, Damian J. Hussey, and Richard Hummel
Clinical Science, 2015, Volume 128, Number 1, Page 1
Violaine K. Harris and Saud A. Sadiq
Molecular Diagnosis & Therapy, 2014, Volume 18, Number 6, Page 605
Tek N. Lamichhane, Sonja Sokic, John S. Schardt, Rahul S. Raiker, Jennifer W. Lin, and Steven M. Jay
Tissue Engineering Part B: Reviews, 2015, Volume 21, Number 1, Page 45
Romain Wyss, Luigino Grasso, Camille Wolf, Wolfgang Grosse, Davide Demurtas, and Horst Vogel
Analytical Chemistry, 2014, Volume 86, Number 15, Page 7229
Anne Louise Schacht Revenfeld, Rikke Bæk, Morten Hjuler Nielsen, Allan Stensballe, Kim Varming, and Malene Jørgensen
Clinical Therapeutics, 2014, Volume 36, Number 6, Page 830
Fatemeh Momen-Heravi, Shashi Bala, Terence Bukong, and Gyongyi Szabo
Nanomedicine: Nanotechnology, Biology and Medicine, 2014, Volume 10, Number 7, Page 1517
Shidong Jia, Davide Zocco, Michael L Samuels, Michael F Chou, Roger Chammas, Johan Skog, Natasa Zarovni, Fatemeh Momen-Heravi, and Winston Patrick Kuo
Expert Review of Molecular Diagnostics, 2014, Volume 14, Number 3, Page 307
Crislyn D'Souza-Schorey and Dolores Di Vizio
Expert Review of Proteomics, 2014, Volume 11, Number 3, Page 251
Xi Yang, Zuquan Weng, Donna L. Mendrick, and Qiang Shi
Toxicology Letters, 2014, Volume 225, Number 3, Page 401

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