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Article: Optimization of Mechanical Tissue Dissociation Using an Integrated Microfluidic Device for Improved Generation of Single Cells Following Digestion.

Aliaghaei, Marzieh / Haun, Jered B

Frontiers in bioengineering and biotechnology

2022 Volume 10, Page(s) 841046

Abstract: The dissociation of tissue and cell aggregates into single cells is of high interest for single cell analysis studies, primary cultures, tissue engineering, and regenerative medicine. However, current methods are slow, poorly controlled, variable, and ... ...

Abstract	The dissociation of tissue and cell aggregates into single cells is of high interest for single cell analysis studies, primary cultures, tissue engineering, and regenerative medicine. However, current methods are slow, poorly controlled, variable, and can introduce artifacts. We previously developed a microfluidic device that contains two separate dissociation modules, a branching channel array and nylon mesh filters, which was used as a polishing step after tissue processing with a microfluidic digestion device. Here, we employed the integrated disaggregation and filtration (IDF) device as a standalone method with both cell aggregates and traditionally digested tissue to perform a well-controlled and detailed study into the effect of mechanical forces on dissociation, including modulation of flow rate, device pass number, and even the mechanism. Using a strongly cohesive cell aggregate model, we found that single cell recovery was highest using flow rates exceeding 40 ml/min and multiple passes through the filter module, either with or without the channel module. For minced and digested kidney tissue, recovery of diverse cell types was maximal using multiple passes through the channel module and only a single pass through the filter module. Notably, we found that epithelial cell recovery from the optimized IDF device alone exceeded our previous efforts, and this result was maintained after reducing digestion time to 20 min. However, endothelial cells and leukocytes still required extended digestion time for maximal recover. These findings highlight the significance of parameter optimization to achieve the highest cell yield and viability based on tissue sample size, extracellular matrix content, and strength of cell-cell interactions.
Language	English
Publishing date	2022-02-08
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2719493-0
ISSN	2296-4185
ISSN	2296-4185
DOI	10.3389/fbioe.2022.841046
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Article ; Online: Microfluidic Device Technologies for Digestion, Disaggregation, and Filtration of Tissue Samples for Single Cell Applications.

Lombardo, Jeremy A / Haun, Jered B

Methods in molecular biology (Clifton, N.J.)

2022 Volume 2394, Page(s) 81–92

Abstract: There is growing interest in breaking down tissues into the individual cellular constituents so that those cells can be identified, assayed for functional characteristics, or utilized for therapeutic purposes. A major driver is the development of single ... ...

Abstract	There is growing interest in breaking down tissues into the individual cellular constituents so that those cells can be identified, assayed for functional characteristics, or utilized for therapeutic purposes. A major driver is the development of single cell analysis methods, which are best poised to assess cellular heterogeneity and discover rare cells. Current tissue dissociation methods are inefficient, produce variable results, and require many labor-intensive, time-consuming steps. To address these shortcomings, we have developed three different microfluidic technologies to perform the critical steps of tissue digestion, disaggregation, and filtration with improved dissociation efficiency and speed. These devices will make it possible to process tissue into single cells for various downstream applications in a rapid and automated fashion.
MeSH term(s)	Digestion ; Filtration ; Lab-On-A-Chip Devices ; Microfluidic Analytical Techniques ; Microfluidics
Language	English
Publishing date	2022-01-30
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-1811-0_6
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Article ; Online: Multiplexed Immunoassay Using Quantum Dots to Monitor Proteins Secreted from Single Cells at Near-Single Molecule Resolution.

Naveen, Veena Y / Deng, Tingwei / Herrera, Vanessa / Haun, Jered B

Methods in molecular biology (Clifton, N.J.)

2023 Volume 2660, Page(s) 187–206

Abstract: Single-cell secretion studies find important applications in molecular diagnostics, therapeutic target identification, and basic biology research. One increasingly important area of research is non-genetic cellular heterogeneity, a phenomenon that can be ...

Abstract	Single-cell secretion studies find important applications in molecular diagnostics, therapeutic target identification, and basic biology research. One increasingly important area of research is non-genetic cellular heterogeneity, a phenomenon that can be studied by assessing secretion of soluble effector proteins from single cells. This is particularly impactful for immune cells, as secreted proteins such as cytokines, chemokines, and growth factors are the gold standard for identifying phenotype. Current methods that rely upon immunofluorescence suffer from low detection sensitivity, requiring thousands of molecules to be secreted per cell. We have developed a quantum dot (QD)-based single-cell secretion analysis platform that can be used in different sandwich immunoassay formats to dramatically lower detection threshold, such that only one to a few molecules need be secreted per cell. We have also expanded this work to include multiplexing capabilities for different cytokines and employed this platform to study macrophage polarization under different stimuli at the single-cell level.
MeSH term(s)	Quantum Dots ; Cytokines ; Immunoassay/methods
Chemical Substances	Cytokines
Language	English
Publishing date	2023-05-16
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-3163-8_13
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Article ; Online: Quantifying and controlling bond multivalency for advanced nanoparticle targeting to cells.

Makhani, Elliot Y / Zhang, Ailin / Haun, Jered B

Nano convergence

2021 Volume 8, Issue 1, Page(s) 38

Abstract: Nanoparticles have drawn intense interest as delivery agents for diagnosing and treating various cancers. Much of the early success was driven by passive targeting mechanisms such as the enhanced permeability and retention (EPR) effect, but this has ... ...

Abstract	Nanoparticles have drawn intense interest as delivery agents for diagnosing and treating various cancers. Much of the early success was driven by passive targeting mechanisms such as the enhanced permeability and retention (EPR) effect, but this has failed to lead to the expected clinical successes. Active targeting involves binding interactions between the nanoparticle and cancer cells, which promotes tumor cell-specific accumulation and internalization. Furthermore, nanoparticles are large enough to facilitate multiple bond formation, which can improve adhesive properties substantially in comparison to the single bond case. While multivalent binding is universally believed to be an attribute of nanoparticles, it is a complex process that is still poorly understood and difficult to control. In this review, we will first discuss experimental studies that have elucidated roles for parameters such as nanoparticle size and shape, targeting ligand and target receptor densities, and monovalent binding kinetics on multivalent nanoparticle adhesion efficiency and cellular internalization. Although such experimental studies are very insightful, information is limited and confounded by numerous differences across experimental systems. Thus, we focus the second part of the review on theoretical aspects of binding, including kinetics, biomechanics, and transport physics. Finally, we discuss various computational and simulation studies of nanoparticle adhesion, including advanced treatments that compare directly to experimental results. Future work will ideally continue to combine experimental data and advanced computational studies to extend our knowledge of multivalent adhesion, as well as design the most powerful nanoparticle-based agents to treat cancer.
Language	English
Publishing date	2021-11-30
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2760386-6
ISSN	2196-5404 ; 2196-5404
ISSN (online)	2196-5404
ISSN	2196-5404
DOI	10.1186/s40580-021-00288-1
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Article ; Online: Fluidic Device System for Mechanical Processing and Filtering of Human Lipoaspirate Enhances Recovery of Mesenchymal Stem Cells.

Lombardo, Jeremy A / Banyard, Derek A / Widgerow, Alan D / Haun, Jered B

Plastic and reconstructive surgery

2022 Volume 151, Issue 1, Page(s) 72e–84e

Abstract: Background: Adipose tissue is an easily accessible source of stem and progenitor cells that offers exciting promise as an injectable autologous therapeutic for regenerative applications. Mechanical processing is preferred over enzymatic digestion, and ... ...

Abstract	Background: Adipose tissue is an easily accessible source of stem and progenitor cells that offers exciting promise as an injectable autologous therapeutic for regenerative applications. Mechanical processing is preferred over enzymatic digestion, and the most common method involves shuffling lipoaspirate between syringes and filtering to produce nanofat. Although nanofat has shown exciting clinical results, the authors hypothesized that new device designs could enhance recovery of stem/progenitor cells through optimization of fluid dynamics principles, integration, and automation. Methods: The authors designed and fabricated the emulsification and micronization device (EMD) and the filtration device (FD) to replace the manual nanofat procedures. Using human lipoaspirate samples, the EMD and the FD were optimized and compared to traditional nanofat using ex vivo measurements of cell number, viability, and percentage of mesenchymal stem cells and endothelial progenitor cells. Results: The EMD produced results statistically similar to nanofat, and these findings were confirmed for a cohort of diabetic patients. Combining the FD with the EMD was superior to manually filtered nanofat in terms of both recovered cell percentages (>1.5-fold) and numbers (two- to three-fold). Differences were statistically significant for total mesenchymal stem cells and a DPP4 + /CD55 + subpopulation linked to improved wound healing in diabetes. Conclusions: The new EMD and the FD improved mechanical processing of human lipoaspirate in terms of mesenchymal stem cell enrichment and number compared to traditional nanofat. Future work will seek to investigate the wound healing response both in vitro and in vivo, and to refine the technology for automated operation within clinical settings. Clinical relevance statement: The new devices improved mechanical processing of human lipoaspirate in terms of stem cell enrichment and number compared to traditional methods. Future work will seek to validate wound healing response and refine the technology for automated operation within clinical settings.
MeSH term(s)	Humans ; Adipocytes ; Adipose Tissue ; Mesenchymal Stem Cells/physiology ; Lipectomy/methods ; Stem Cells
Language	English
Publishing date	2022-10-07
Publishing country	United States
Document type	Journal Article
ZDB-ID	208012-6
ISSN	1529-4242 ; 0032-1052 ; 0096-8501
ISSN (online)	1529-4242
ISSN	0032-1052 ; 0096-8501
DOI	10.1097/PRS.0000000000009798
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Article ; Online: Microfluidic platform accelerates tissue processing into single cells for molecular analysis and primary culture models.

Lombardo, Jeremy A / Aliaghaei, Marzieh / Nguyen, Quy H / Kessenbrock, Kai / Haun, Jered B

Nature communications

2021 Volume 12, Issue 1, Page(s) 2858

Abstract: Tissues are complex mixtures of different cell subtypes, and this diversity is increasingly characterized using high-throughput single cell analysis methods. However, these efforts are hindered, as tissues must first be dissociated into single cell ... ...

Abstract	Tissues are complex mixtures of different cell subtypes, and this diversity is increasingly characterized using high-throughput single cell analysis methods. However, these efforts are hindered, as tissues must first be dissociated into single cell suspensions using methods that are often inefficient, labor-intensive, highly variable, and potentially biased towards certain cell subtypes. Here, we present a microfluidic platform consisting of three tissue processing technologies that combine tissue digestion, disaggregation, and filtration. The platform is evaluated using a diverse array of tissues. For kidney and mammary tumor, microfluidic processing produces 2.5-fold more single cells. Single cell RNA sequencing further reveals that endothelial cells, fibroblasts, and basal epithelium are enriched without affecting stress response. For liver and heart, processing time is dramatically reduced. We also demonstrate that recovery of cells from the system at periodic intervals during processing increases hepatocyte and cardiomyocyte numbers, as well as increases reproducibility from batch-to-batch for all tissues.
MeSH term(s)	Animals ; Cell Count ; Endothelial Cells/cytology ; Endothelial Cells/metabolism ; Fibroblasts/cytology ; Fibroblasts/metabolism ; Hepatocytes/cytology ; Hepatocytes/metabolism ; Humans ; Kidney/cytology ; Kidney/metabolism ; Liver/cytology ; Liver/metabolism ; MCF-7 Cells ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Microfluidic Analytical Techniques/instrumentation ; Microfluidic Analytical Techniques/methods ; Myocardium/cytology ; Myocardium/metabolism ; Myocytes, Cardiac/cytology ; Myocytes, Cardiac/metabolism ; Reproducibility of Results ; Sequence Analysis, RNA/methods ; Single-Cell Analysis/methods ; Mice
Language	English
Publishing date	2021-05-17
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-23238-1
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Article ; Online: Multiplexed Detection of Secreted Cytokines at near-Molecular Resolution Elucidates Macrophage Polarization Heterogeneity.

Herrera, Vanessa / Hsu, Ssu-Chieh Joseph / Naveen, Veena Y / Liu, Wendy F / Haun, Jered B

Analytical chemistry

2021 Volume 94, Issue 2, Page(s) 658–668

Abstract: Monitoring the secretion of proteins from single cells can provide important insights into how cells respond to their microenvironment. This is particularly true for immune cells, which can exhibit a large degree of response heterogeneity. ... ...

Abstract	Monitoring the secretion of proteins from single cells can provide important insights into how cells respond to their microenvironment. This is particularly true for immune cells, which can exhibit a large degree of response heterogeneity. Microfabricated well arrays provide a powerful and versatile method to assess the secretion of cytokines, chemokines, and growth factors from single cells, but detection sensitivity has been limited to high levels on the order of 10,000 per cell. Recently, we reported a quantum dot-based immunoassay that lowered the detection limit for the cytokine TNF-α to concentrations to nearly the single-cell level. Here, we adapted this detection method to three additional targets while maintaining high detection sensitivity. Specifically, we detected MCP-1, TGF-β, IL-10, and TNF-α using quantum dots with different emission spectra, each of which displayed a detection threshold in the range of 1-10 fM or ∼1-2 molecules per well. We then quantified secretion of all four proteins from single macrophage cells that were stimulated toward a pro-inflammatory state with lipopolysaccharide (LPS) or toward a pro-healing state with both LPS and interleukin 4 (IL-4). We found that MCP-1 and TGF-β were predominantly secreted at high levels only (>10,000 molecules/cell), while a substantial number of cells secreted IL-10 and TNF-α at lower levels that could only be detected using our method. Subsequent principal component and cluster analysis revealed that secretion profiles could be classified as either exclusively pro-inflammatory, including MCP-1 and/or TNF-α, or more subtle responses displaying both pro-healing and pro-inflammatory characters. Our results highlight the heterogeneous and nondiscrete nature of macrophage phenotypes following
MeSH term(s)	Cytokines/analysis ; Immunoassay/methods ; Lipopolysaccharides/pharmacology ; Macrophages/chemistry ; Tumor Necrosis Factor-alpha/analysis
Chemical Substances	Cytokines ; Lipopolysaccharides ; Tumor Necrosis Factor-alpha
Language	English
Publishing date	2021-12-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1508-8
ISSN	1520-6882 ; 0003-2700
ISSN (online)	1520-6882
ISSN	0003-2700
DOI	10.1021/acs.analchem.1c02222
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Article ; Online: Extracting multivalent detachment rates from heterogeneous nanoparticle populations.

Wang, Mingqiu / Allard, Jun / Haun, Jered B

Physical chemistry chemical physics : PCCP

2018 Volume 20, Issue 33, Page(s) 21430–21440

Abstract: Nanoparticles can form multiple bonds with target surfaces, thereby increasing adhesion strength and internalization rate into cells. This property has helped to drive interest in nanoparticles as delivery vehicles for drugs and imaging agents, but ... ...

Abstract	Nanoparticles can form multiple bonds with target surfaces, thereby increasing adhesion strength and internalization rate into cells. This property has helped to drive interest in nanoparticles as delivery vehicles for drugs and imaging agents, but significant gaps in our understanding of multivalent adhesion make it difficult to control and optimize binding dynamics. In previous work, we experimentally observed that multivalent nanoparticle adhesion can exhibit a time-dependent detachment rate. However, simulations later indicated that the underlying cause was variability in the number of bonds that formed between individual nanoparticles within the population. Here, we use this insight to develop a simple model to isolate a series of constant detachment rates from such heterogeneous populations. Using simulations of experimental data to train the model, we first classified nanoparticles within a given population based on the most likely equilibrium bond number, which we termed the bond potential. We then assumed that each bond potential category would follow standard first-order kinetics with constant detachment rates. Model results matched the population binding data, but only if we further divided each bond potential category into two sub-components, the second of which did not detach. We then utilized bonding rates from the simulation to estimate detachment rates for the second, slower detaching sub-component. These results confirm our hypothesis that nanoparticle populations can be sub-divided based on bond potential, each of which could be characterized by a constant detachment rate. Finally, we established relationships between the new heterogeneous population detachment model and a time-dependent, empirical detachment model that we developed in previous work. This could make it possible to determine bond potential distributions directly from experimental data without computationally costly simulations, which will be explored in future work.
Language	English
Publishing date	2018-08-07
Publishing country	England
Document type	Journal Article
ZDB-ID	1476244-4
ISSN	1463-9084 ; 1463-9076
ISSN (online)	1463-9084
ISSN	1463-9076
DOI	10.1039/c8cp03118e
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Article: Multiplexed Detection of Secreted Cytokines at near-Molecular Resolution Elucidates Macrophage Polarization Heterogeneity

Herrera, Vanessa / Hsu, Ssu-Chieh Joseph / Naveen, Veena Y. / Liu, Wendy F. / Haun, Jered B.

Analytical chemistry. 2021 Dec. 22, v. 94, no. 2

2021

Abstract	Monitoring the secretion of proteins from single cells can provide important insights into how cells respond to their microenvironment. This is particularly true for immune cells, which can exhibit a large degree of response heterogeneity. Microfabricated well arrays provide a powerful and versatile method to assess the secretion of cytokines, chemokines, and growth factors from single cells, but detection sensitivity has been limited to high levels on the order of 10,000 per cell. Recently, we reported a quantum dot-based immunoassay that lowered the detection limit for the cytokine TNF-α to concentrations to nearly the single-cell level. Here, we adapted this detection method to three additional targets while maintaining high detection sensitivity. Specifically, we detected MCP-1, TGF-β, IL-10, and TNF-α using quantum dots with different emission spectra, each of which displayed a detection threshold in the range of 1–10 fM or ∼1–2 molecules per well. We then quantified secretion of all four proteins from single macrophage cells that were stimulated toward a pro-inflammatory state with lipopolysaccharide (LPS) or toward a pro-healing state with both LPS and interleukin 4 (IL-4). We found that MCP-1 and TGF-β were predominantly secreted at high levels only (>10,000 molecules/cell), while a substantial number of cells secreted IL-10 and TNF-α at lower levels that could only be detected using our method. Subsequent principal component and cluster analysis revealed that secretion profiles could be classified as either exclusively pro-inflammatory, including MCP-1 and/or TNF-α, or more subtle responses displaying both pro-healing and pro-inflammatory characters. Our results highlight the heterogeneous and nondiscrete nature of macrophage phenotypes following in vitro stimulation of a cell line. Future work will focus on expanding the multiplexing capacity by extending emission spectra bandwidth and/or spatially barcoding capture antibodies, as well as evaluating the enhanced detection sensitivity capabilities with normal and diseased immune cell populations in vitro and in vivo.
Keywords	analytical chemistry ; barcoding ; cell lines ; chemokines ; cluster analysis ; detection limit ; immunoassays ; interleukin-10 ; interleukin-4 ; lipopolysaccharides ; macrophages ; quantum dots
Language	English
Dates of publication	2021-1222
Size	p. 658-668.
Publishing place	American Chemical Society
Document type	Article
ZDB-ID	1508-8
ISSN	1520-6882 ; 0003-2700
ISSN (online)	1520-6882
ISSN	0003-2700
DOI	10.1021/acs.analchem.1c02222
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Phasor Analysis of Fluorescence Lifetime Enables Quantitative Multiplexed Molecular Imaging of Three Probes.

Rahim, Maha K / Zhao, Jinghui / Patel, Hinesh V / Lagouros, Hauna A / Kota, Rajesh / Fernandez, Irma / Gratton, Enrico / Haun, Jered B

Analytical chemistry

2022 Volume 94, Issue 41, Page(s) 14185–14194

Abstract: The excited-state lifetime is an intrinsic property of fluorescent molecules that can be leveraged for multiplexed imaging. An advantage of fluorescence lifetime-based multiplexing is that signals from multiple probes can be gathered simultaneously, ... ...

Abstract	The excited-state lifetime is an intrinsic property of fluorescent molecules that can be leveraged for multiplexed imaging. An advantage of fluorescence lifetime-based multiplexing is that signals from multiple probes can be gathered simultaneously, whereas traditional spectral fluorescence imaging typically requires multiple images at different excitation and emission wavelengths. Additionally, lifetime and spectra could both be utilized to expand the multiplexing capacity of fluorescence. However, resolving exogenous molecular probes based exclusively on the fluorescence lifetime has been limited by technical challenges in analyzing lifetime data. The phasor approach to lifetime analysis offers a simple, graphical solution that has increasingly been used to assess endogenous cellular autofluorescence to quantify metabolic factors. In this study, we employed the phasor analysis of FLIM to quantitatively resolve three exogenous, antibody-targeted fluorescent probes with similar spectral properties based on lifetime information alone. First, we demonstrated that three biomarkers that were spatially restricted to the cell membrane, cytosol, or nucleus could be accurately distinguished using FLIM and phasor analysis. Next, we successfully resolved and quantified three probes that were all targeted to cell surface biomarkers. Finally, we demonstrated that lifetime-based quantitation accuracy can be improved through intensity matching of various probe-biomarker combinations, which will expand the utility of this technique. Importantly, we reconstructed images for each individual probe, as well as an overlay of all three probes, from a single FLIM image. Our results demonstrate that FLIM and phasor analysis can be leveraged as a powerful tool for simultaneous detection of multiple biomarkers with high sensitivity and accuracy.
MeSH term(s)	Fluorescent Dyes ; Microscopy, Fluorescence/methods ; Molecular Imaging ; Molecular Probes ; Optical Imaging
Chemical Substances	Fluorescent Dyes ; Molecular Probes
Language	English
Publishing date	2022-10-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1508-8
ISSN	1520-6882 ; 0003-2700
ISSN (online)	1520-6882
ISSN	0003-2700
DOI	10.1021/acs.analchem.2c02149
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