Spatially-Resolved Proteomics: Rapid Quantitative Analysis of Laser Capture Microdissected Alveolar Tissue Samples

Clair, Geremy; Piehowski, Paul D.; Nicola, Teodora; Kitzmiller, Joseph A.; Huang, Eric L.; Zink, Erika M.; Sontag, Ryan L.; Orton, Daniel J.; Moore, Ronald J.; Carson, James P.; Smith, Richard D.; Whitsett, Jeffrey A.; Corley, Richard A.; Ambalavanan, Namasivayam; Ansong, Charles

doi:10.1038/srep39223

Title: Spatially-Resolved Proteomics: Rapid Quantitative Analysis of Laser Capture Microdissected Alveolar Tissue Samples

Journal Article · Thu Dec 22 00:00:00 EST 2016 · Scientific Reports

DOI:https://doi.org/10.1038/srep39223· OSTI ID:1340766

Clair, Geremy ^[1]; Piehowski, Paul D. ^[1]; Nicola, Teodora ^[2]; Kitzmiller, Joseph A. ^[3]; Huang, Eric L. ^[1]; Zink, Erika M. ^[1]; Sontag, Ryan L. ^[1]; Orton, Daniel J. ^[1]; Moore, Ronald J. ^[1]; Carson, James P. ^[4]; Smith, Richard D. ^[1]; Whitsett, Jeffrey A. ^[3]; Corley, Richard A. ^[1]; Ambalavanan, Namasivayam ^[2]; Ansong, Charles ^[1]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Univ. of Alabama, Birmingham, AL (United States)
Cincinnati Children’s Hospital Medical Center, Cincinnati, OH (United States)
Univ. of Texas, Austin, TX (United States)

Global proteomics approaches allow characterization of whole tissue lysates to an impressive depth. However, it is now increasingly recognized that to better understand the complexity of multicellular organisms, global protein profiling of specific spatially defined regions/substructures of tissues (i.e. spatially-resolved proteomics) is essential. Laser capture microdissection (LCM) enables microscopic isolation of defined regions of tissues preserving crucial spatial information. However, current proteomics workflows entail several manual sample preparation steps and are challenged by the microscopic mass-limited samples generated by LCM, and that impact measurement robustness, quantification, and throughput. Here, we coupled LCM with a fully automated sample preparation workflow that with a single manual step allows: protein extraction, tryptic digestion, peptide cleanup and LC-MS/MS analysis of proteomes from microdissected tissues. Benchmarking against the current state of the art in ultrasensitive global proteomic analysis, our approach demonstrated significant improvements in quantification and throughput. Using our LCM-SNaPP proteomics approach, we characterized to a depth of more than 3,400 proteins, the ontogeny of protein changes during normal lung development in laser capture microdissected alveolar tissue containing ~4,000 cells per sample. Importantly, the data revealed quantitative changes for 350 low abundance transcription factors and signaling molecules, confirming earlier transcript-level observations and defining seven modules of coordinated transcription factor/signaling molecule expression patterns, suggesting that a complex network of temporal regulatory control directs normal lung development with epigenetic regulation fine-tuning pre-natal developmental processes. Furthermore, our LCM-proteomics approach facilitates efficient, spatially-resolved, ultrasensitive global proteomics analyses in high-throughput that will be enabling for several clinical and biological applications.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1340766

Report Number(s):: PNNL-SA-119185; 48632; 453040220

Journal Information:: Scientific Reports, Vol. 6; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 54 works

Citation information provided by
Web of Science

References (71)

Multidimensional proteomics for cell biology Larance, Mark; Lamond, Angus I. Nature Reviews Molecular Cell Biology, Vol. 16, Issue 5 https://doi.org/10.1038/nrm3970	journal	April 2015
Application of immobilized enzyme reactor in on-line high performance liquid chromatography: A review Girelli, Anna Maria; Mattei, Enrico Journal of Chromatography B, Vol. 819, Issue 1 https://doi.org/10.1016/j.jchromb.2005.01.031	journal	May 2005
Comparative Reevaluation of FASP and Enhanced FASP Methods by LC–MS/MS Nel, Andrew J. M.; Garnett, Shaun; Blackburn, Jonathan M. Journal of Proteome Research, Vol. 14, Issue 3 https://doi.org/10.1021/pr501266c	journal	February 2015
Surfactant proteins SP-A and SP-D: Structure, function and receptors Kishore, Uday; Greenhough, Trevor J.; Waters, Patrick Molecular Immunology, Vol. 43, Issue 9 https://doi.org/10.1016/j.molimm.2005.08.004	journal	March 2006
Epigenetic Regulation of miR-17∼92 Contributes to the Pathogenesis of Pulmonary Fibrosis Dakhlallah, Duaa; Batte, Kara; Wang, Yijie American Journal of Respiratory and Critical Care Medicine, Vol. 187, Issue 4 https://doi.org/10.1164/rccm.201205-0888OC	journal	February 2013
TGF-β signaling is dynamically regulated during the alveolarization of rodent and human lungs Alejandre-Alcázar, Miguel A.; Michiels-Corsten, Matthias; Vicencio, Alfin G. Developmental Dynamics, Vol. 237, Issue 1 https://doi.org/10.1002/dvdy.21403	journal	January 2007
Spin filter–based sample preparation for shotgun proteomics Liebler, Daniel C.; Ham, Amy-Joan L. Nature Methods, Vol. 6, Issue 11 https://doi.org/10.1038/nmeth1109-785a	journal	November 2009
Spatially resolved transcriptomics and beyond Crosetto, Nicola; Bienko, Magda; van Oudenaarden, Alexander Nature Reviews Genetics, Vol. 16, Issue 1 https://doi.org/10.1038/nrg3832	journal	December 2014
Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq Treutlein, Barbara; Brownfield, Doug G.; Wu, Angela R. Nature, Vol. 509, Issue 7500 https://doi.org/10.1038/nature13173	journal	April 2014
Proteomics-based identification of low-abundance signaling and regulatory protein complexes in native plant tissues Smaczniak, Cezary; Li, Na; Boeren, Sjef Nature Protocols, Vol. 7, Issue 12 https://doi.org/10.1038/nprot.2012.129	journal	November 2012
Lung development: orchestrating the generation and regeneration of a complex organ Herriges, M.; Morrisey, E. E. Development, Vol. 141, Issue 3 https://doi.org/10.1242/dev.098186	journal	January 2014
Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells Kulak, Nils A.; Pichler, Garwin; Paron, Igor Nature Methods, Vol. 11, Issue 3 https://doi.org/10.1038/nmeth.2834	journal	February 2014
Lung growth and development Chinoy, Mala R. Frontiers in Bioscience, Vol. 8, Issue 4 https://doi.org/10.2741/974	journal	January 2003
Transcriptional Programs Controlling Perinatal Lung Maturation Xu, Yan; Wang, Yanhua; Besnard, Valérie PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0037046	journal	August 2012
High Recovery FASP Applied to the Proteomic Analysis of Microdissected Formalin Fixed Paraffin Embedded Cancer Tissues Retrieves Known Colon Cancer Markers Wiśniewski, Jacek R.; Ostasiewicz, Pawel; Mann, Matthias Journal of Proteome Research, Vol. 10, Issue 7 https://doi.org/10.1021/pr200019m	journal	July 2011
Age, Sexual Dimorphism, and Disease Associations in the Developing Human Fetal Lung Transcriptome Kho, Alvin T.; Chhabra, Divya; Sharma, Sunita American Journal of Respiratory Cell and Molecular Biology, Vol. 54, Issue 6 https://doi.org/10.1165/rcmb.2015-0326OC	journal	June 2016
Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801 https://doi.org/10.1021/ac061133r	journal	November 2006
Integrated Capillary Zone Electrophoresis–Electrospray Ionization Tandem Mass Spectrometry System with an Immobilized Trypsin Microreactor for Online Digestion and Analysis of Picogram Amounts of RAW 264.7 Cell Lysate Sun, Liangliang; Zhu, Guijie; Dovichi, Norman J. Analytical Chemistry, Vol. 85, Issue 8 https://doi.org/10.1021/ac400523x	journal	March 2013
Inhibitory effect of receptor for advanced glycation end products (RAGE) on the TGF-β-induced alveolar epithelial to mesenchymal transition Song, Jeong Sup; Kang, Chun Mi; Park, Chan Kwon Experimental and Molecular Medicine, Vol. 43, Issue 9 https://doi.org/10.3858/emm.2011.43.9.059	journal	January 2011
Liver carboxylesterase cleaves surfactant protein (SP-) B and promotes surfactant subtype conversion Ruppert, Clemens; Bagheri, Ariane; Markart, Philipp Biochemical and Biophysical Research Communications, Vol. 348, Issue 4 https://doi.org/10.1016/j.bbrc.2006.08.013	journal	October 2006
Expression Profiling of the Developing Mouse Lung: Insights into the Establishment of the Extracellular Matrix Mariani, Thomas J.; Reed, Jeremy J.; Shapiro, Steven D. American Journal of Respiratory Cell and Molecular Biology, Vol. 26, Issue 5 https://doi.org/10.1165/ajrcmb.26.5.2001-00080c	journal	May 2002
Tissue Proteomics for the Next Decade? Towards a Molecular Dimension in Histology Longuespée, Rémi; Fléron, Maximilien; Pottier, Charles OMICS: A Journal of Integrative Biology, Vol. 18, Issue 9 https://doi.org/10.1089/omi.2014.0033	journal	September 2014
More Sensitive and Quantitative Proteomic Measurements Using Very Low Flow Rate Porous Silica Monolithic LC Columns with Electrospray Ionization-Mass Spectrometry Luo, Quanzhou; Tang, Keqi; Yang, Feng Journal of Proteome Research, Vol. 5, Issue 5 https://doi.org/10.1021/pr050424y	journal	May 2006
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Cox, Jürgen; Mann, Matthias Nature Biotechnology, Vol. 26, Issue 12 https://doi.org/10.1038/nbt.1511	journal	November 2008
Lung Surfactant Levels are Regulated by Ig-Hepta/GPR116 by Monitoring Surfactant Protein D Fukuzawa, Taku; Ishida, Junji; Kato, Akira PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069451	journal	July 2013
Gpr116 Receptor Regulates Distinctive Functions in Pneumocytes and Vascular Endothelium Niaudet, Colin; Hofmann, Jennifer J.; Mäe, Maarja A. PLOS ONE, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pone.0137949	journal	September 2015
The Molecular Era of Surfactant Biology Whitsett, Jeffrey A. Neonatology, Vol. 105, Issue 4 https://doi.org/10.1159/000360649	journal	January 2014
The Q Exactive HF, a Benchtop Mass Spectrometer with a Pre-filter, High-performance Quadrupole and an Ultra-high-field Orbitrap Analyzer Scheltema, Richard Alexander; Hauschild, Jan-Peter; Lange, Oliver Molecular & Cellular Proteomics, Vol. 13, Issue 12 https://doi.org/10.1074/mcp.M114.043489	journal	October 2014
Systems biology approaches to identify developmental bases for lung diseases Bhattacharya, Soumyaroop; Mariani, Thomas J. Pediatric Research, Vol. 73, Issue 2-4 https://doi.org/10.1038/pr.2013.7	journal	January 2013
Sources of Technical Variability in Quantitative LC–MS Proteomics: Human Brain Tissue Sample Analysis Piehowski, Paul D.; Petyuk, Vladislav A.; Orton, Daniel J. Journal of Proteome Research, Vol. 12, Issue 5 https://doi.org/10.1021/pr301146m	journal	April 2013
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
Transcriptional Control of Lung Morphogenesis Maeda, Yutaka; Davé, Vrushank; Whitsett, Jeffrey A. Physiological Reviews, Vol. 87, Issue 1 https://doi.org/10.1152/physrev.00028.2006	journal	January 2007
Gene Targeting of the Cysteine Peptidase Cathepsin H Impairs Lung Surfactant in Mice Bühling, Frank; Kouadio, Martin; Chwieralski, Caroline E. PLoS ONE, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pone.0026247	journal	October 2011
Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ Cox, Jürgen; Hein, Marco Y.; Luber, Christian A. Molecular & Cellular Proteomics, Vol. 13, Issue 9 https://doi.org/10.1074/mcp.M113.031591	journal	June 2014
Quantitative proteomic analysis of single pancreatic islets Waanders, Leonie F.; Chwalek, Karolina; Monetti, Mara Proceedings of the National Academy of Sciences, Vol. 106, Issue 45 https://doi.org/10.1073/pnas.0908351106	journal	October 2009
Quantitative Proteomic Analysis of Microdissected Breast Cancer Tissues: Comparison of Label-Free and SILAC-based Quantification with Shotgun, Directed, and Targeted MS Approaches Liu, Ning Qing; Dekker, Lennard J. M.; Stingl, Christoph Journal of Proteome Research, Vol. 12, Issue 10 https://doi.org/10.1021/pr4005794	journal	September 2013
Differential Recovery of Peptides from Sample Tubes and the Reproducibility of Quantitative Proteomic Data Bark, Steven J.; Hook, Vivian Journal of Proteome Research, Vol. 6, Issue 11 https://doi.org/10.1021/pr070294o	journal	November 2007
SNaPP: Simplified Nanoproteomics Platform for Reproducible Global Proteomic Analysis of Nanogram Protein Quantities Huang, Eric L.; Piehowski, Paul D.; Orton, Daniel J. Endocrinology, Vol. 157, Issue 3 https://doi.org/10.1210/en.2015-1821	journal	March 2016
High-Efficiency Nanoscale Liquid Chromatography Coupled On-Line with Mass Spectrometry Using Nanoelectrospray Ionization for Proteomics Shen, Yufeng; Zhao, Rui; Berger, Scott J. Analytical Chemistry, Vol. 74, Issue 16 https://doi.org/10.1021/ac0202280	journal	August 2002
Temporal-spatial distribution of SP-B and SP-C proteins and mRNAs in developing respiratory epithelium of human lung. Khoor, A.; Stahlman, M. T.; Gray, M. E. Journal of Histochemistry & Cytochemistry, Vol. 42, Issue 9 https://doi.org/10.1177/42.9.8064126	journal	September 1994
Universal sample preparation method for proteome analysis Wiśniewski, Jacek R.; Zougman, Alexandre; Nagaraj, Nagarjuna Nature Methods, Vol. 6, Issue 5 https://doi.org/10.1038/nmeth.1322	journal	April 2009
Epithelial–mesenchymal transition in lung development and disease: does it exist and is it important? Bartis, Domokos; Mise, Nikica; Mahida, Rahul Y. Thorax, Vol. 69, Issue 8 https://doi.org/10.1136/thoraxjnl-2013-204608	journal	December 2013
Cathepsin H and napsin A are active in the alveoli and increased in alveolar proteinosis Woischnik, M.; Bauer, A.; Aboutaam, R. European Respiratory Journal, Vol. 31, Issue 6 https://doi.org/10.1183/09031936.00081207	journal	March 2008
Trends in ultrasensitive proteomics Altelaar, AF Maarten; Heck, Albert JR Current Opinion in Chemical Biology, Vol. 16, Issue 1-2 https://doi.org/10.1016/j.cbpa.2011.12.011	journal	April 2012
Surfactant-Aided Precipitation/on-Pellet-Digestion (SOD) Procedure Provides Robust and Rapid Sample Preparation for Reproducible, Accurate and Sensitive LC/MS Quantification of Therapeutic Protein in Plasma and Tissues An, Bo; Zhang, Ming; Johnson, Robert W. Analytical Chemistry, Vol. 87, Issue 7 https://doi.org/10.1021/acs.analchem.5b00350	journal	March 2015
Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition Rock, J. R.; Barkauskas, C. E.; Cronce, M. J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 52 https://doi.org/10.1073/pnas.1117988108	journal	November 2011
Ultrasensitive proteome analysis using paramagnetic bead technology Hughes, Christopher S.; Foehr, Sophia; Garfield, David A. Molecular Systems Biology, Vol. 10, Issue 10 https://doi.org/10.15252/msb.20145625	journal	October 2014
Positional proteomics in the era of the human proteome project on the doorstep of precision medicine Eckhard, Ulrich; Marino, Giada; Butler, Georgina S. Biochimie, Vol. 122 https://doi.org/10.1016/j.biochi.2015.10.018	journal	March 2016
Growth hormone (GH) receptor knockout mice reveal actions of GH in lung development Beyea, Jason A.; Sawicki, Grzegorz; Olson, David M. PROTEOMICS, Vol. 6, Issue 1 https://doi.org/10.1002/pmic.200500168	journal	January 2006
Imaging mass spectrometry: Hype or hope? Heeren, Ron M. A.; Smith, Donald F.; Stauber, Jonathan Journal of the American Society for Mass Spectrometry, Vol. 20, Issue 6 https://doi.org/10.1016/j.jasms.2009.01.011	journal	June 2009
Microproteomics: Analysis of protein diversity in small samples Gutstein, Howard B.; Morris, Jeffrey S.; Annangudi, Suresh P. Mass Spectrometry Reviews, Vol. 27, Issue 4 https://doi.org/10.1002/mas.20161	journal	January 2008
Developmental alveolarization of the mouse lung Mund, Sonja I.; Stampanoni, Marco; Schittny, Johannes C. Developmental Dynamics, Vol. 237, Issue 8 https://doi.org/10.1002/dvdy.21633	journal	August 2008
Foxp2 and Foxp1 cooperatively regulate lung and esophagus development Shu, W.; Lu, M. M.; Zhang, Y. Development, Vol. 134, Issue 10 https://doi.org/10.1242/dev.02846	journal	April 2007
Epigenetic Regulation of Surfactant Protein A Gene (SP-A) Expression in Fetal Lung Reveals a Critical Role for Suv39h Methyltransferases during Development and Hypoxia Benlhabib, H.; Mendelson, C. R. Molecular and Cellular Biology, Vol. 31, Issue 10 https://doi.org/10.1128/MCB.01063-10	journal	March 2011
Cadherin-6B stimulates an epithelial mesenchymal transition and the delamination of cells from the neural ectoderm via LIMK/cofilin mediated non-canonical BMP receptor signaling Park, Ki-Sook; Gumbiner, Barry M. Developmental Biology, Vol. 366, Issue 2 https://doi.org/10.1016/j.ydbio.2012.04.005	journal	June 2012
Open Tubular Lab-On-Column/Mass Spectrometry for Targeted Proteomics of Nanogram Sample Amounts Hustoft, Hanne Kolsrud; Vehus, Tore; Brandtzaeg, Ole Kristian PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0106881	journal	September 2014
Plasticity of Hopx+ type I alveolar cells to regenerate type II cells in the lung Jain, Rajan; Barkauskas, Christina E.; Takeda, Norifumi Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7727	journal	April 2015
Molecular mechanisms of epithelial–mesenchymal transition Lamouille, Samy; Xu, Jian; Derynck, Rik Nature Reviews Molecular Cell Biology, Vol. 15, Issue 3 https://doi.org/10.1038/nrm3758	journal	February 2014
Matrix effects in biological mass spectrometry imaging: identification and compensation Lanekoff, Ingela; Stevens, Susan L.; Stenzel-Poore, Mary P. The Analyst, Vol. 139, Issue 14 https://doi.org/10.1039/c4an00504j	journal	January 2014
Self-made frits for nanoscale columns in proteomics Maiolica, Alessio; Borsotti, Dario; Rappsilber, Juri PROTEOMICS, Vol. 5, Issue 15 https://doi.org/10.1002/pmic.200402010	journal	October 2005
DA-Raf-dependent inhibition of the Ras-ERK signaling pathway in type 2 alveolar epithelial cells controls alveolar formation Watanabe-Takano, H.; Takano, K.; Sakamoto, A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1321574111	journal	May 2014
Enzyme-immobilized reactors for rapid and efficient sample preparation in MS-based proteomic studies Yamaguchi, Hiroshi; Miyazaki, Masaya PROTEOMICS, Vol. 13, Issue 3-4 https://doi.org/10.1002/pmic.201200272	journal	January 2013
Integrated proteomic and transcriptomic profiling of mouse lung development and Nmyc target genes Cox, Brian; Kislinger, Thomas; Wigle, Dennis A. Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100151	journal	January 2007
Transcriptional Programs Controlling Perinatal Lung Maturation Xu, Yan; Wang, Yanhua; Besnard, Valerie American Thoracic Society 2012 International Conference, May 18-23, 2012 • San Francisco, California, A28. LUNG DEVELOPMENT: BENCH TO BEDSIDE https://doi.org/10.1164/ajrccm-conference.2012.185.1_meetingabstracts.a1216	conference	May 2012
Lung Growth and Development O'Brodovich, Hugh ACCP/AAP Pediatric Pulmonary Medicine Board Review: 1st Edition https://doi.org/10.1378/ppmbr.1st.001	book	January 2010
Network of Dynamic Interactions between Histone H1 and High-Mobility-Group Proteins in Chromatin Catez, F.; Yang, H.; Tracey, K. J. Molecular and Cellular Biology, Vol. 24, Issue 10 https://doi.org/10.1128/mcb.24.10.4321-4328.2004	journal	April 2004
Transcriptional and DNA Binding Activity of the Foxp1/2/4 Family Is Modulated by Heterotypic and Homotypic Protein Interactions Li, S.; Weidenfeld, J.; Morrisey, E. E. Molecular and Cellular Biology, Vol. 24, Issue 2 https://doi.org/10.1128/mcb.24.2.809-822.2004	journal	December 2003
Proteomic Analysis of Lung Tissue in a Rat Acute Lung Injury Model: Identification of PRDX1 as a Promoter of Inflammation Liu, Dongdong; Mao, Pu; Huang, Yongbo Mediators of Inflammation, Vol. 2014 https://doi.org/10.1155/2014/469358	journal	January 2014
The Promise of Epigenetic Therapies in Treatment of Idiopathic Pulmonary Fibrosis Rosas, Ivan O.; Yang, Ivana V. American Journal of Respiratory and Critical Care Medicine, Vol. 187, Issue 4 https://doi.org/10.1164/rccm.201212-2272ed	journal	February 2013
Orphan G Protein–Coupled Receptor GPR116 Regulates Pulmonary Surfactant Pool Size Bridges, James P.; Ludwig, Marie-Gabrielle; Mueller, Matthias American Journal of Respiratory Cell and Molecular Biology, Vol. 49, Issue 3 https://doi.org/10.1165/rcmb.2012-0439oc	journal	September 2013
Effects of growth hormone-releasing hormone and its agonistic and antagonistic analogs in cancer and non-cancerous cell lines International Journal of Oncology, Vol. 36, Issue 5 https://doi.org/10.3892/ijo_00000613	journal	March 2010

Cited By (23)

Proteomic Analysis of Single Mammalian Cells Enabled by Microfluidic Nanodroplet Sample Preparation and Ultrasensitive NanoLC-MS Zhu, Ying; Clair, Geremy; Chrisler, William B. Angewandte Chemie, Vol. 130, Issue 38 https://doi.org/10.1002/ange.201802843	journal	June 2018
Proteomic Analysis of Single Mammalian Cells Enabled by Microfluidic Nanodroplet Sample Preparation and Ultrasensitive NanoLC-MS Zhu, Ying; Clair, Geremy; Chrisler, William B. Angewandte Chemie International Edition, Vol. 57, Issue 38 https://doi.org/10.1002/anie.201802843	journal	June 2018
Collagen analysis with mass spectrometry Huizen, Nick A.; Ijzermans, Jan N. M.; Burgers, Peter C. Mass Spectrometry Reviews, Vol. 39, Issue 4 https://doi.org/10.1002/mas.21600	journal	September 2019
Benchtop-compatible sample processing workflow for proteome profiling of < 100 mammalian cells Xu, Kerui; Liang, Yiran; Piehowski, Paul D. Analytical and Bioanalytical Chemistry, Vol. 411, Issue 19 https://doi.org/10.1007/s00216-018-1493-9	journal	November 2018
A transcriptomic atlas of aged human microglia Olah, Marta; Patrick, Ellis; Villani, Alexandra-Chloe Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-02926-5	journal	February 2018
Nanodroplet processing platform for deep and quantitative proteome profiling of 10–100 mammalian cells Zhu, Ying; Piehowski, Paul D.; Zhao, Rui Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03367-w	journal	February 2018
Automated mass spectrometry imaging of over 2000 proteins from tissue sections at 100-μm spatial resolution Piehowski, Paul D.; Zhu, Ying; Bramer, Lisa M. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-13858-z	journal	January 2020
Cell type-resolved human lung lipidome reveals cellular cooperation in lung function Kyle, Jennifer E.; Clair, Geremy; Bandyopadhyay, Gautam Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-31640-x	journal	September 2018
Facile carrier-assisted targeted mass spectrometric approach for proteomic analysis of low numbers of mammalian cells Shi, Tujin; Gaffrey, Matthew J.; Fillmore, Thomas L. Communications Biology, Vol. 1, Issue 1 https://doi.org/10.1038/s42003-018-0107-6	journal	August 2018
Increased β-cell proliferation before immune cell invasion prevents progression of type 1 diabetes Dirice, Ercument; Kahraman, Sevim; De Jesus, Dario F. Nature Metabolism, Vol. 1, Issue 5 https://doi.org/10.1038/s42255-019-0061-8	journal	May 2019
New mass spectrometry technologies contributing towards comprehensive and high throughput omics analyses of single cells Couvillion, Sneha P.; Zhu, Ying; Nagy, Gabe The Analyst, Vol. 144, Issue 3 https://doi.org/10.1039/c8an01574k	journal	January 2019
Nanoproteomics comes of age Zhu, Ying; Piehowski, Paul D.; Kelly, Ryan T. Expert Review of Proteomics, Vol. 15, Issue 11 https://doi.org/10.1080/14789450.2018.1537787	journal	October 2018
The role of proteomics in assessing beta-cell dysfunction and death in type 1 diabetes Nakayasu, Ernesto S.; Qian, Wei-Jun; Evans-Molina, Carmella Expert Review of Proteomics, Vol. 16, Issue 7 https://doi.org/10.1080/14789450.2019.1634548	journal	June 2019
LungMAP: The Molecular Atlas of Lung Development Program Ardini-Poleske, Maryanne E.; Clark, Robert F.; Ansong, Charles American Journal of Physiology-Lung Cellular and Molecular Physiology, Vol. 313, Issue 5 https://doi.org/10.1152/ajplung.00139.2017	journal	November 2017
Recent advances in our understanding of the mechanisms of late lung development and bronchopulmonary dysplasia Surate Solaligue, David E.; Rodríguez-Castillo, José Alberto; Ahlbrecht, Katrin American Journal of Physiology-Lung Cellular and Molecular Physiology, Vol. 313, Issue 6 https://doi.org/10.1152/ajplung.00343.2017	journal	December 2017
A multiomics focusing towards the molecular networks of lung development Clair, Geremy American Journal of Physiology-Lung Cellular and Molecular Physiology, Vol. 317, Issue 5 https://doi.org/10.1152/ajplung.00364.2019	journal	November 2019
Integration of transcriptomic and proteomic data identifies biological functions in cell populations from human infant lung Du, Yina; Clair, Geremy C.; Al Alam, Denise American Journal of Physiology-Lung Cellular and Molecular Physiology, Vol. 317, Issue 3 https://doi.org/10.1152/ajplung.00475.2018	journal	September 2019
Glomerular filtrate proteins in acute cardiorenal syndrome Wakasaki, Rumie; Matsushita, Katsuyuki; Golgotiu, Kirsti JCI Insight, Vol. 4, Issue 4 https://doi.org/10.1172/jci.insight.122130	journal	February 2019
Proteomic Biomarkers for the Detection of Endometrial Cancer Njoku, Kelechi; Chiasserini, Davide; Whetton, Anthony D. Cancers, Vol. 11, Issue 10 https://doi.org/10.3390/cancers11101572	journal	October 2019
A transcriptomic atlas of aged human microglia Olah, Marta; Patrick, Ellis; Villani, Alexandra-Chloe Columbia University https://doi.org/10.7916/d8tm8t6b	text	January 2018
Nipah Virus-Like Particle Egress Is Modulated by Cytoskeletal and Vesicular Trafficking Pathways: a Validated Particle Proteomics Analysis Johnston, Gunner P.; Bradel-Tretheway, Birgit; Piehowski, Paul D. mSystems, Vol. 4, Issue 5 https://doi.org/10.1128/msystems.00194-19	journal	October 2019
Application of a Sensitive and Reproducible Label-Free Proteomic Approach to Explore the Proteome of Individual Meiotic-Phase Barley Anthers Lewandowska, Dominika; Zhang, Runxuan; Colas, Isabelle Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00393	journal	April 2019
Micropuncture of Bowman's Space in Mice Facilitated by 2 Photon Microscopy Matsushita, Katsuyuki; Golgotiu, Kirsti; Orton, Daniel J. Journal of Visualized Experiments, Issue 140 https://doi.org/10.3791/58206-v	journal	October 2018

Similar Records

Spatially Resolved Proteome Mapping of Laser Capture Microdissected Tissue with Automated Sample Transfer to Nanodroplets

Journal Article · Sun Jun 24 00:00:00 EDT 2018 · Molecular and Cellular Proteomics · OSTI ID:1340766

Zhu, Ying; Dou, Maowei; Piehowski, Paul D.; +12 more

Spatially Resolved Proteome Mapping of Laser Capture Microdissected Tissue with Automated Sample Transfer to Nanodroplets

Journal Article · Sat Sep 01 00:00:00 EDT 2018 · Molecular and Cellular Proteomics · OSTI ID:1340766

Zhu, Ying; Dou, Maowei; Piehowski, Paul D.; +12 more

Cell-Type-Specific Proteomics Analysis of a Small Number of Plant Cells by Integrating Laser Capture Microdissection with a Nanodroplet Sample Processing Platform

Journal Article · Thu May 27 00:00:00 EDT 2021 · Current Protocols · OSTI ID:1340766

Balasubramanian, Vimal K.; Purvine, Samuel O.; Liang, Yiran; +7 more

Related Subjects

60 APPLIED LIFE SCIENCES
Environmental Molecular Sciences Laboratory

Title: Spatially-Resolved Proteomics: Rapid Quantitative Analysis of Laser Capture Microdissected Alveolar Tissue Samples

Citation Formats

References (71)

Cited By (23)

Similar Records

Related Subjects