A proteome-wide assessment of the oxidative stress paradigm for metal and metal-oxide nanomaterials in human macrophages
Abstract
Responsible implementation of engineered nanomaterials (ENMs) into commercial applications is an important societal issue, driving demand for new approaches for rapid and comprehensive evaluation of their bioactivity and safety. An essential part of any research focused on identifying potential hazard of ENMs is the appropriate selection of biological endpoints to evaluate. Herein, we use a tiered strategy employing both targeted biological assays and untargeted quantitative proteomics to elucidate the biological responses of human macrophages across a library of metal/metal oxide ENMs, raised as priority ENMs for investigation by NIEHS’s Nanomaterial Health Implications Research (NHIR) program. Our results show that quantitative cellular proteome profiles readily distinguish ENM types based on their cytotoxic potential according to induction of biological processes and pathways involved in the cellular antioxidant response, TCA cycle, oxidative stress, endoplasmic reticulum stress, and immune responses as major processes impacted. Interestingly, pathway analysis of differentially abundant proteins also revealed new cell processes that were influenced by all ENMs independent of cytotoxic potential. These included pathways previously implicated as cellular adaptive mechanisms to low levels of oxidative stress, including cell adhesion, protein translation and protein targeting pathways. Unsupervised clustering of all data revealed the most striking proteome changes that differentiated ENMmore »
- Authors:
-
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH); Nanotechnology Health Implications Research (NHIR) Consortium
- OSTI Identifier:
- 1642069
- Report Number(s):
- PNNL-SA-147217
Journal ID: ISSN 2452-0748
- Grant/Contract Number:
- AC05-76RL01830; UO1ES027292; P41GM103494; U24ES026946
- Resource Type:
- Accepted Manuscript
- Journal Name:
- NanoImpact
- Additional Journal Information:
- Journal Volume: 17; Journal ID: ISSN 2452-0748
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE; Engineered nanomaterials, proteomics, cytotoxicity, oxidative stress, macrophage
Citation Formats
Zhang, Tong, Gaffrey, Matthew J., Thomas, Dennis G., Weber, Thomas J., Hess, Becky M., Weitz, Karl K., Piehowski, Paul D., Petyuk, Vladislav A., Moore, Ronald J., Qian, Wei-Jun, and Thrall, Brian D. A proteome-wide assessment of the oxidative stress paradigm for metal and metal-oxide nanomaterials in human macrophages. United States: N. p., 2019.
Web. doi:10.1016/j.impact.2019.100194.
Zhang, Tong, Gaffrey, Matthew J., Thomas, Dennis G., Weber, Thomas J., Hess, Becky M., Weitz, Karl K., Piehowski, Paul D., Petyuk, Vladislav A., Moore, Ronald J., Qian, Wei-Jun, & Thrall, Brian D. A proteome-wide assessment of the oxidative stress paradigm for metal and metal-oxide nanomaterials in human macrophages. United States. https://doi.org/10.1016/j.impact.2019.100194
Zhang, Tong, Gaffrey, Matthew J., Thomas, Dennis G., Weber, Thomas J., Hess, Becky M., Weitz, Karl K., Piehowski, Paul D., Petyuk, Vladislav A., Moore, Ronald J., Qian, Wei-Jun, and Thrall, Brian D. Sat .
"A proteome-wide assessment of the oxidative stress paradigm for metal and metal-oxide nanomaterials in human macrophages". United States. https://doi.org/10.1016/j.impact.2019.100194. https://www.osti.gov/servlets/purl/1642069.
@article{osti_1642069,
title = {A proteome-wide assessment of the oxidative stress paradigm for metal and metal-oxide nanomaterials in human macrophages},
author = {Zhang, Tong and Gaffrey, Matthew J. and Thomas, Dennis G. and Weber, Thomas J. and Hess, Becky M. and Weitz, Karl K. and Piehowski, Paul D. and Petyuk, Vladislav A. and Moore, Ronald J. and Qian, Wei-Jun and Thrall, Brian D.},
abstractNote = {Responsible implementation of engineered nanomaterials (ENMs) into commercial applications is an important societal issue, driving demand for new approaches for rapid and comprehensive evaluation of their bioactivity and safety. An essential part of any research focused on identifying potential hazard of ENMs is the appropriate selection of biological endpoints to evaluate. Herein, we use a tiered strategy employing both targeted biological assays and untargeted quantitative proteomics to elucidate the biological responses of human macrophages across a library of metal/metal oxide ENMs, raised as priority ENMs for investigation by NIEHS’s Nanomaterial Health Implications Research (NHIR) program. Our results show that quantitative cellular proteome profiles readily distinguish ENM types based on their cytotoxic potential according to induction of biological processes and pathways involved in the cellular antioxidant response, TCA cycle, oxidative stress, endoplasmic reticulum stress, and immune responses as major processes impacted. Interestingly, pathway analysis of differentially abundant proteins also revealed new cell processes that were influenced by all ENMs independent of cytotoxic potential. These included pathways previously implicated as cellular adaptive mechanisms to low levels of oxidative stress, including cell adhesion, protein translation and protein targeting pathways. Unsupervised clustering of all data revealed the most striking proteome changes that differentiated ENM classes involved a small subset of proteins involved in the oxidative stess response (HMOX1), protein chaperone functions (HS71B, DNJB1), and autophagy (SQSTM), providing a potential new panel of markers of ENM-induced cell stress. To our knowledge, the results represent the most comprehensive profiling of the biological responses to a library of ENMs conducted using quantitative mass spectrometry-based proteomics. The results provide a basis to identify the patterns of a diverse set of cellular pathways and cell processes impacted by ENM exposure in an important immune cell type, laying the foundation for multivariate, pathway-level structure activity assessments of ENMs in the future.},
doi = {10.1016/j.impact.2019.100194},
journal = {NanoImpact},
number = ,
volume = 17,
place = {United States},
year = {2019},
month = {11}
}
Web of Science
Works referenced in this record:
Mussel-inspired 3D fiber scaffolds for heart-on-a-chip toxicity studies of engineered nanomaterials
journal, May 2018
- Ahn, Seungkuk; Ardoña, Herdeline Ann M.; Lind, Johan U.
- Analytical and Bioanalytical Chemistry, Vol. 410, Issue 24
Actin-binding protein alpha-actinin 4 (ACTN4) is a transcriptional co-activator of RelA/p65 sub-unit of NF-kB
journal, February 2013
- Aksenova, Vasilisa; Turoverova, Lidia; Khotin, Mikhail
- Oncotarget, Vol. 4, Issue 2
Role of metal oxide nanoparticles in histopathological changes observed in the lung of welders
journal, January 2014
- Andujar, Pascal; Simon-Deckers, Angélique; Galateau-Sallé, Françoise
- Particle and Fibre Toxicology, Vol. 11, Issue 1
Development of reference metal and metal oxide engineered nanomaterials for nanotoxicology research using high throughput and precision flame spray synthesis approaches
journal, April 2018
- Beltran-Huarac, Juan; Zhang, Zhenyuan; Pyrgiotakis, Georgios
- NanoImpact, Vol. 10
Multi-hierarchical profiling the structure-activity relationships of engineered nanomaterials at nano-bio interfaces
journal, October 2018
- Cai, Xiaoming; Dong, Jun; Liu, Jing
- Nature Communications, Vol. 9, Issue 1
Endoplasmic Reticulum Stress Induced by Zinc Oxide Nanoparticles Is an Earlier Biomarker for Nanotoxicological Evaluation
journal, February 2014
- Chen, Rui; Huo, Lingling; Shi, Xiaofei
- ACS Nano, Vol. 8, Issue 3
Parallel Comparative Studies on Mouse Toxicity of Oxide Nanoparticle- and Gadolinium-Based T1 MRI Contrast Agents
journal, November 2015
- Chen, Rui; Ling, Daishun; Zhao, Lin
- ACS Nano, Vol. 9, Issue 12
Reactive oxygen species as essential mediators of cell adhesion
journal, June 2003
- Chiarugi, Paola; Pani, Giovambattista; Giannoni, Elisa
- Journal of Cell Biology, Vol. 161, Issue 5
Lobar pneumonia: an occupational disease in welders
journal, July 1994
- Coggon, D.
- The Lancet, Vol. 344, Issue 8914
Transcriptional profiling reveals gene expression changes associated with inflammation and cell proliferation following short-term inhalation exposure to copper oxide nanoparticles
journal, November 2017
- Costa, Pedro M.; Gosens, Ilse; Williams, Andrew
- Journal of Applied Toxicology, Vol. 38, Issue 3
Preparation, characterization, and in vitro dosimetry of dispersed, engineered nanomaterials
journal, January 2017
- DeLoid, Glen M.; Cohen, Joel M.; Pyrgiotakis, Georgios
- Nature Protocols, Vol. 12, Issue 2
Proinflammatory Effects of Pyrogenic and Precipitated Amorphous Silica Nanoparticles in Innate Immunity Cells
journal, November 2015
- Di Cristo, Luisana; Movia, Dania; Bianchi, Massimiliano G.
- Toxicological Sciences, Vol. 150, Issue 1
Quantitative Profiling of Protein S-Glutathionylation Reveals Redox-Dependent Regulation of Macrophage Function during Nanoparticle-Induced Oxidative Stress
journal, December 2015
- Duan, Jicheng; Kodali, Vamsi K.; Gaffrey, Matthew J.
- ACS Nano, Vol. 10, Issue 1
Oxidative stress and autophagy: the clash between damage and metabolic needs
journal, September 2014
- Filomeni, G.; De Zio, D.; Cecconi, F.
- Cell Death & Differentiation, Vol. 22, Issue 3
Role of omics techniques in the toxicity testing of nanoparticles
journal, November 2017
- Fröhlich, Eleonore
- Journal of Nanobiotechnology, Vol. 15, Issue 1
PMA-Induced THP-1 Macrophage Differentiation is Not Impaired by Citrate-Coated Platinum Nanoparticles
journal, October 2017
- Gatto, Francesca; Cagliani, Roberta; Catelani, Tiziano
- Nanomaterials, Vol. 7, Issue 10
Regulation of Translation by Hydrogen Peroxide
journal, July 2011
- Grant, Chris M.
- Antioxidants & Redox Signaling, Vol. 15, Issue 1
NF-κB Is a Negative Regulator of IL-1β Secretion as Revealed by Genetic and Pharmacological Inhibition of IKKβ
journal, September 2007
- Greten, Florian R.; Arkan, Melek C.; Bollrath, Julia
- Cell, Vol. 130, Issue 5
Unfolding the relationship between secreted molecular chaperones and macrophage activation states
journal, October 2008
- Henderson, Brian; Henderson, Samantha
- Cell Stress and Chaperones, Vol. 14, Issue 4
Roles of Heat Shock Proteins in Apoptosis, Oxidative Stress, Human Inflammatory Diseases, and Cancer
journal, December 2017
- Ikwegbue, Paul; Masamba, Priscilla; Oyinloye, Babatunji
- Pharmaceuticals, Vol. 11, Issue 1
p62/ SQSTM1 and Selective Autophagy in Cardiometabolic Diseases
journal, August 2019
- Jeong, Se-Jin; Zhang, Xiangyu; Rodriguez-Velez, Astrid
- Antioxidants & Redox Signaling, Vol. 31, Issue 6
Short Communication Transient increase in IL-1β, IL-6 and TNF-α gene expression in rat liver exposed to gold nanoparticles
journal, January 2013
- Khan, H. A.; Abdelhalim, M. A. K.; Alhomida, A. S.
- Genetics and Molecular Research, Vol. 12, Issue 4
Zinc Oxide Nanoparticles Suppress LPS-Induced NF- κ B Activation by Inducing A20, a Negative Regulator of NF- κ B, in RAW 264.7 Macrophages
journal, September 2015
- Kim, Min-Ho; Jeong, Hyun-Ja
- Journal of Nanoscience and Nanotechnology, Vol. 15, Issue 9
Effects of copper nanoparticle exposure on host defense in a murine pulmonary infection model
journal, January 2011
- Kim, Jong Sung; Adamcakova-Dodd, Andrea; O'Shaughnessy, Patrick T.
- Particle and Fibre Toxicology, Vol. 8, Issue 1
Comparative toxicity of 24 manufactured nanoparticles in human alveolar epithelial and macrophage cell lines
journal, January 2009
- Lanone, Sophie; Rogerieux, Françoise; Geys, Jorina
- Particle and Fibre Toxicology, Vol. 6, Issue 1
Dysregulation of Macrophage Activation Profiles by Engineered Nanoparticles
journal, July 2013
- Kodali, Vamsi; Littke, Matthew H.; Tilton, Susan C.
- ACS Nano, Vol. 7, Issue 8
Inflammatory and Oxidative Stress Responses of an Alveolar Epithelial Cell Line to Airborne Zinc Oxide Nanoparticles at the Air-Liquid Interface: A Comparison with Conventional, Submerged Cell-Culture Conditions
journal, January 2013
- Lenz, Anke-Gabriele; Karg, Erwin; Brendel, Ellen
- BioMed Research International, Vol. 2013
Estimation of Electronegativity Values of Elements in Different Valence States
journal, October 2006
- Li, Keyan; Xue, Dongfeng
- The Journal of Physical Chemistry A, Vol. 110, Issue 39
New insights into the roles of CHOP-induced apoptosis in ER stress
journal, August 2014
- Li, Yiming; Guo, Yunshan; Tang, Juan
- Acta Biochimica et Biophysica Sinica, Vol. 46, Issue 8
Rack1, a Receptor for Activated Protein Kinase C, Interacts with Integrin β Subunit
journal, January 1998
- Liliental, Joanna; Chang, David D.
- Journal of Biological Chemistry, Vol. 273, Issue 4
Quantitative Proteomic Analysis to Understand the Mechanisms of Zinc Oxide Nanoparticle Toxicity to Daphnia pulex (Crustacea: Daphniidae): Comparing with Bulk Zinc Oxide and Zinc Salt
journal, April 2019
- Lin, Li; Xu, Mingzhi; Mu, Huawei
- Environmental Science & Technology, Vol. 53, Issue 9
Environmental Risk Factors for Community-Acquired Pneumonia Hospitalization in Older Adults: PNEUMONIA IN OLDER ADULTS
journal, June 2009
- Loeb, Mark; Neupane, Binod; Walter, Stephen D.
- Journal of the American Geriatrics Society, Vol. 57, Issue 6
Gold nanoparticles attenuate LPS-induced NO production through the inhibition of NF-κB and IFN-β/STAT1 pathways in RAW264.7 cells
journal, November 2010
- Ma, Ji Su; Kim, Wan Jae; Kim, Jae Jin
- Nitric Oxide, Vol. 23, Issue 3
Gold Nanoparticles Induce Autophagosome Accumulation through Size-Dependent Nanoparticle Uptake and Lysosome Impairment
journal, October 2011
- Ma, Xiaowei; Wu, Yanyang; Jin, Shubin
- ACS Nano, Vol. 5, Issue 11
A Predictive Toxicological Paradigm for the Safety Assessment of Nanomaterials
journal, June 2009
- Meng, Huan; Xia, Tian; George, Saji
- ACS Nano, Vol. 3, Issue 7
Intracellular accumulation dynamics and fate of zinc ions in alveolar epithelial cells exposed to airborne ZnO nanoparticles at the air–liquid interface
journal, November 2013
- Mihai, Cosmin; Chrisler, William B.; Xie, Yumei
- Nanotoxicology, Vol. 9, Issue 1
Responses of human cells to ZnO nanoparticles: a gene transcription study
journal, January 2011
- Moos, Philip J.; Olszewski, Kyle; Honeggar, Matthew
- Metallomics, Vol. 3, Issue 11
Toxic Potential of Materials at the Nanolevel
journal, February 2006
- Nel, A.
- Science, Vol. 311, Issue 5761
Long-Term Exposure to Ambient Air Pollution and Risk of Hospitalization with Community-acquired Pneumonia in Older Adults
journal, January 2010
- Neupane, Binod; Jerrett, Michael; Burnett, Richard T.
- American Journal of Respiratory and Critical Care Medicine, Vol. 181, Issue 1
Co-translational targeting and translocation of proteins to the endoplasmic reticulum
journal, November 2013
- Nyathi, Yvonne; Wilkinson, Barrie M.; Pool, Martin R.
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1833, Issue 11
Exposure to Metal Fume and Infectious Pneumonia
journal, February 2003
- Palmer, K. T.
- American Journal of Epidemiology, Vol. 157, Issue 3
Nanoparticles: a boon to drug delivery, therapeutics, diagnostics and imaging
journal, February 2012
- Parveen, Suphiya; Misra, Ranjita; Sahoo, Sanjeeb K.
- Nanomedicine: Nanotechnology, Biology and Medicine, Vol. 8, Issue 2
Differences in gene expression and cytokine production by crystalline vs. amorphous silica in human lung epithelial cells
journal, January 2012
- Perkins, Timothy N.; Shukla, Arti; Peeters, Paul M.
- Particle and Fibre Toxicology, Vol. 9, Issue 1
Regulated Expression of Integrins and Other Adhesion Molecules during Differentiation of Monocytes into Macrophages
journal, June 1994
- Prieto, Jacqueline; Eklund, Anders; Patarroyo, Manuel
- Cellular Immunology, Vol. 156, Issue 1
Using nano-QSAR to predict the cytotoxicity of metal oxide nanoparticles
journal, February 2011
- Puzyn, Tomasz; Rasulev, Bakhtiyor; Gajewicz, Agnieszka
- Nature Nanotechnology, Vol. 6, Issue 3
Cytotoxicity and global transcriptional responses induced by zinc oxide nanoparticles NM 110 in PMA-differentiated THP-1 cells
journal, June 2019
- Safar, Ramia; Doumandji, Zahra; Saidou, Timeh
- Toxicology Letters, Vol. 308
Silver Nanoparticle Protein Corona Composition in Cell Culture Media
journal, September 2013
- Shannahan, Jonathan H.; Lai, Xianyin; Ke, Pu Chun
- PLoS ONE, Vol. 8, Issue 9
Nanotechnology: An Untapped Resource for Food Packaging
journal, September 2017
- Sharma, Chetan; Dhiman, Romika; Rokana, Namita
- Frontiers in Microbiology, Vol. 8
Global Translational Responses to Oxidative Stress Impact upon Multiple Levels of Protein Synthesis
journal, July 2006
- Shenton, Daniel; Smirnova, Julia B.; Selley, Julian N.
- Journal of Biological Chemistry, Vol. 281, Issue 39
Adaptation to stress in yeast: to translate or not?
journal, July 2012
- Simpson, Clare E.; Ashe, Mark P.
- Biochemical Society Transactions, Vol. 40, Issue 4
SWAP-70 Regulates c-kit-Induced Mast Cell Activation, Cell-Cell Adhesion, and Migration
journal, December 2004
- Sivalenka, Raja Rajeswari; Jessberger, Rolf
- Molecular and Cellular Biology, Vol. 24, Issue 23
All that is silver is not toxic: silver ion and particle kinetics reveals the role of silver ion aging and dosimetry on the toxicity of silver nanoparticles
journal, December 2018
- Smith, Jordan N.; Thomas, Dennis G.; Jolley, Hadley
- Particle and Fibre Toxicology, Vol. 15, Issue 1
Repeated exposure to iron oxide nanoparticles causes testicular toxicity in mice: TOXIC EFFECTS OF IRON OXIDE NANOPARTICLES ON MICE TESTIS
journal, March 2016
- Sundarraj, Kiruthika; Manickam, Vijayprakash; Raghunath, Azhwar
- Environmental Toxicology, Vol. 32, Issue 2
Iron oxide nanoparticles modulate heat shock proteins and organ specific markers expression in mice male accessory organs
journal, February 2017
- Sundarraj, Kiruthika; Raghunath, Azhwar; Panneerselvam, Lakshmikanthan
- Toxicology and Applied Pharmacology, Vol. 317
Intracellular accumulation of indium ions released from nanoparticles induces oxidative stress, proinflammatory response and DNA damage
journal, September 2015
- Tabei, Yosuke; Sonoda, Akinari; Nakajima, Yoshihiro
- Journal of Biochemistry, Vol. 159, Issue 2
Nuclear Heat Shock Protein 72 as a Negative Regulator of Oxidative Stress (Hydrogen Peroxide)-Induced HMGB1 Cytoplasmic Translocation and Release
journal, May 2007
- Tang, Daolin; Kang, Rui; Xiao, Weimin
- The Journal of Immunology, Vol. 178, Issue 11
Cytotoxic and Proinflammatory Effects of Metal-Based Nanoparticles on THP-1 Monocytes Characterized by Combined Proteomics Approaches
journal, December 2016
- Tarasova, Nataliya K.; Gallud, Audrey; Ytterberg, A. Jimmy
- Journal of Proteome Research, Vol. 16, Issue 2
ISD3: a particokinetic model for predicting the combined effects of particle sedimentation, diffusion and dissolution on cellular dosimetry for in vitro systems
journal, January 2018
- Thomas, Dennis G.; Smith, Jordan N.; Thrall, Brian D.
- Particle and Fibre Toxicology, Vol. 15, Issue 1
Modulation of susceptibility to lung bacterial infection by engineered nanomaterials: In vitro and in vivo correspondence based on macrophage phagocytic function
journal, February 2019
- Thrall, Brian D.; Kodali, Vamsi; Skerrett, Shawn
- NanoImpact, Vol. 14
Alarmin High Mobility Group Box 1 (HMGB1) Activates Alternative NFkB Signaling in Bone Marrow Macrophages in the Leukemia Microenvironment
journal, December 2015
- Toia, Liana M.; Mariano, John; Winter, Michael Weinstein
- Blood, Vol. 126, Issue 23
Quantitative proteomics identifies redox switches for global translation modulation by mitochondrially produced reactive oxygen species
journal, January 2018
- Topf, Ulrike; Suppanz, Ida; Samluk, Lukasz
- Nature Communications, Vol. 9, Issue 1
Identification of the Nanogold Particle-Induced Endoplasmic Reticulum Stress by Omic Techniques and Systems Biology Analysis
journal, November 2011
- Tsai, Yen-Yin; Huang, Yi-Huei; Chao, Ya-Li
- ACS Nano, Vol. 5, Issue 12
Protein aggregation as a cellular response to oxidative stress induced by heme and iron
journal, November 2016
- Vasconcellos, Luiz R. C.; Dutra, Fabianno F.; Siqueira, Mariana S.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 47
Photocatalytic Reactive Oxygen Species Formation by Semiconductor–Metal Hybrid Nanoparticles. Toward Light-Induced Modulation of Biological Processes
journal, May 2016
- Waiskopf, Nir; Ben-Shahar, Yuval; Galchenko, Michael
- Nano Letters, Vol. 16, Issue 7
Exogenous heat shock protein 70 binds macrophage lipid raft microdomain and stimulates phagocytosis, processing, and MHC-II presentation of antigens
journal, February 2006
- Wang, Ruibo; Kovalchin, Joseph T.; Muhlenkamp, Peggy
- Blood, Vol. 107, Issue 4
Quantitative Analysis of Reactive Oxygen Species Photogenerated on Metal Oxide Nanoparticles and Their Bacteria Toxicity: The Role of Superoxide Radicals
journal, August 2017
- Wang, Dan; Zhao, Lixia; Ma, Haiyan
- Environmental Science & Technology, Vol. 51, Issue 17
Macrophage Responses to Silica Nanoparticles are Highly Conserved Across Particle Sizes
journal, December 2008
- Waters, Katrina M.; Masiello, Lisa M.; Zangar, Richard C.
- Toxicological Sciences, Vol. 107, Issue 2
Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1 and IL-1
journal, October 2010
- Yazdi, A. S.; Guarda, G.; Riteau, N.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 45
Quantitative proteomics analysis of adsorbed plasma proteins classifies nanoparticles with different surface properties and size
journal, November 2011
- Zhang, Haizhen; Burnum, Kristin E.; Luna, Maria L.
- PROTEOMICS, Vol. 11, Issue 23
Use of Metal Oxide Nanoparticle Band Gap To Develop a Predictive Paradigm for Oxidative Stress and Acute Pulmonary Inflammation
journal, April 2012
- Zhang, Haiyuan; Ji, Zhaoxia; Xia, Tian
- ACS Nano, Vol. 6, Issue 5
Mass spectrometry-based proteomics for system-level characterization of biological responses to engineered nanomaterials
journal, June 2018
- Zhang, Tong; Gaffrey, Matthew J.; Thrall, Brian D.
- Analytical and Bioanalytical Chemistry, Vol. 410, Issue 24
Quantitative Proteomic Analysis of Cellular Resistance to the Nanoparticle Abraxane
journal, September 2015
- Zhao, Minzhi; Li, Haiyun; Bu, Xiangli
- ACS Nano, Vol. 9, Issue 10
Response gene to complement 32 (RGC-32) expression on M2-polarized and tumor-associated macrophages is M-CSF-dependent and enhanced by tumor-derived IL-4
journal, November 2014
- Zhao, Peng; Gao, Daiqing; Wang, Qingjie
- Cellular & Molecular Immunology, Vol. 12, Issue 6
Scatter Enhanced Phase Contrast Microscopy for Discriminating Mechanisms of Active Nanoparticle Transport in Living Cells
journal, January 2019
- Zimmerman, John F.; Ardoña, Herdeline Ann M.; Pyrgiotakis, Georgios
- Nano Letters, Vol. 19, Issue 2