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6. Untargeted Spatial Metabolomics and Spatial Proteomics on the Same Tissue Section

Author

Vandergrift, Gregory W., Veličković, Marija, Day, Le Z., Gorman, Brittney L., Williams, Sarah M., Shrestha, Bindesh, and Anderton, Christopher R.

Abstract

An increasing number of spatial multiomic workflows have recently been developed. Some of these approaches have leveraged initial mass spectrometry imaging (MSI)-based spatial metabolomics to inform the region of interest (ROI) selection for downstream spatial proteomics. However, these workflows have been limited by varied substrate requirements between modalities or have required analyzing serial sections (i.e., one section per modality). To mitigate these issues, we present a new multiomic workflow that uses desorption electrospray ionization (DESI)-MSI to identify representative spatial metabolite patterns on-tissue prior to spatial proteomic analyses on the same tissue section. This workflow is demonstrated here with a model mammalian tissue (coronal rat brain section) mounted on a poly(ethylene naphthalate)-membrane slide. Initial DESI-MSI resulted in 160 annotations (SwissLipids) within the METASPACE platform (≤20% false discovery rate). A segmentation map from the annotated ion images informed the downstream ROI selection for spatial proteomics characterization from the same sample. The unspecific substrate requirements and minimal sample disruption inherent to DESI-MSI allowed for an optimized, downstream spatial proteomics assay, resulting in 3888 ± 240 to 4717 ± 48 proteins being confidently directed per ROI (200 μm × 200 μm). Finally, we demonstrate the integration of multiomic information, where we found ceramide localization to be correlated with SMPD3 abundance (ceramide synthesis protein), and we also utilized protein abundance to resolve metabolite isomeric ambiguity. Overall, the integration of DESI-MSI into the multiomic workflow allows for complementary spatial- and molecular-level information to be achieved from optimized implementations of each MS assay inherent to the workflow itself.

Published
2025
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8. Proteome-scale tissue mapping using mass spectrometry based on label-free and multiplexed workflows

Author

Kwon, Yumi, primary, Woo, Jongmin, additional, Yu, Fengchao, additional, Williams, Sarah M., additional, Markillie, Lye Meng, additional, Moore, Ronald J., additional, Nakayasu, Ernesto S., additional, Chen, Jing, additional, Campbell-Thompson, Martha, additional, Mathews, Clayton E., additional, Nesvizhskii, Alexey I., additional, Qian, Wei-Jun, additional, and Zhu, Ying, additional

Published
2024
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9. Spatial top-down proteomics for the functional characterization of human kidney

Author

Zemaitis, Kevin J, primary, Fulcher, James M, additional, Kumar, Rashmi, additional, Degnan, David J, additional, Lewis, Logan A, additional, Liao, Yen-Chen, additional, Velickovic, Marija, additional, Williams, Sarah M, additional, Moore, Ronald J, additional, Bramer, Lisa M, additional, Velickovic, Dusan, additional, Zhu, Ying, additional, Zhou, Mowei, additional, and Pasa-Tolic, Ljiljana, additional

Published
2024
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13. Coupling Microdroplet-Based Sample Preparation, Multiplexed Isobaric Labeling, and Nanoflow Peptide Fractionation for Deep Proteome Profiling of the Tissue Microenvironment

Author

Veličković, Marija, Fillmore, Thomas L., Attah, Isaac Kwame, Posso, Camilo, Pino, James C., Zhao, Rui, Williams, Sarah M., Veličković, Dušan, Jacobs, Jon M., Burnum-Johnson, Kristin E., Zhu, Ying, and Piehowski, Paul D.

Abstract

There is increasing interest in developing in-depth proteomic approaches for mapping tissue heterogeneity in a cell-type-specific manner to better understand and predict the function of complex biological systems such as human organs. Existing spatially resolved proteomics technologies cannot provide deep proteome coverage due to limited sensitivity and poor sample recovery. Herein, we seamlessly combined laser capture microdissection with a low-volume sample processing technology that includes a microfluidic device named microPOTS (microdroplet processing in one pot for trace samples), multiplexed isobaric labeling, and a nanoflow peptide fractionation approach. The integrated workflow allowed us to maximize proteome coverage of laser-isolated tissue samples containing nanogram levels of proteins. We demonstrated that the deep spatial proteomics platform can quantify more than 5000 unique proteins from a small-sized human pancreatic tissue pixel (∼60,000 μm2) and differentiate unique protein abundance patterns in pancreas. Furthermore, the use of the microPOTS chip eliminated the requirement for advanced microfabrication capabilities and specialized nanoliter liquid handling equipment, making it more accessible to proteomic laboratories.

Published
2024
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17. Coupling microdroplet-based sample preparation, multiplexed isobaric labeling, and nanoflow peptide fractionation for deep proteome profiling of tissue microenvironment

Author

Veličković, Marija, primary, Fillmore, Thomas L., additional, Attah, Kwame, additional, Posso, Camilo, additional, Pino, James C., additional, Zhao, Rui, additional, Williams, Sarah M., additional, Veličković, Dušan, additional, Jacobs, Jon M., additional, Burnum-Johnson, Kristin E., additional, Zhu, Ying, additional, and Piehowski, Paul D., additional

Published
2023
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20. An optimized approach and inflation media for obtaining complimentary mass spectrometry-based omics data from human lung tissue

Author

Lukowski, Jessica K., primary, Olson, Heather, additional, Velickovic, Marija, additional, Wang, Juan, additional, Kyle, Jennifer E., additional, Kim, Young-Mo, additional, Williams, Sarah M., additional, Zhu, Ying, additional, Huyck, Heidi L., additional, McGraw, Matthew D., additional, Poole, Cory, additional, Rogers, Lisa, additional, Misra, Ravi, additional, Alexandrov, Theodore, additional, Ansong, Charles, additional, Pryhuber, Gloria S., additional, Clair, Geremy, additional, Adkins, Joshua N., additional, Carson, James P., additional, and Anderton, Christopher R., additional

Published
2022
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22. Identification of the genomic mutation in Epha[4.sup.rb-2J/rb-2J] mice

Author

Mohd-Zin, Siti W., Abdullah, Nor-Linda, Abdullah, Aminah, Greene, Nicholas D.E., Cheah, Pike-See, Ling, King-Hwa, Yusof, Hadri, Marwan, Ahmed I., Williams, Sarah M., York, Kerri T., Ahmad-Annuar, Azlina, and Abdul-Aziz, Noraishah M.

Subjects
Gene mutations -- Observations, Tyrosine -- Physiological aspects, Phosphotransferases -- Physiological aspects, Biological sciences
Abstract

The EphA4 receptor tyrosine kinase is involved in numerous cell-signalling activities during embryonic development. EphA4 has the ability to bind to both types of ephrin ligands, the ephrinAs and ephrinBs. [...]

Published
2016

24. Parallel measurement of transcriptomes and proteomes from same single cells using nanodroplet splitting

Author

Fulcher, James M., primary, Markillie, Lye Meng, additional, Mitchell, Hugh D., additional, Williams, Sarah M., additional, Engbrecht, Kristin M., additional, Moore, Ronald J., additional, Cantlon-Bruce, Joshua, additional, Bagnoli, Johannes W., additional, Seth, Anjali, additional, Paša-Tolić, Ljiljana, additional, and Zhu, Ying, additional

Published
2022
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25. Three-dimensional feature matching improves coverage for single-cell proteomics based on ion mobility filtering

Author

Woo, Jongmin, primary, Clair, Geremy C., additional, Williams, Sarah M., additional, Feng, Song, additional, Tsai, Chia-Feng, additional, Moore, Ronald J., additional, Chrisler, William B., additional, Smith, Richard D., additional, Kelly, Ryan T., additional, Paša-Tolić, Ljiljana, additional, Ansong, Charles, additional, and Zhu, Ying, additional

Published
2022
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28. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates

Author

McCurdy, Carrie E., Bishop, Jacalyn M., Williams, Sarah M., Grayson, Bernadette E., Smith, M. Susan, Friedman, Jacob E., and Grove, Kevin L.

Subjects
Ketogenic diet -- Health aspects, Ketogenic diet -- Research, Obesity in children -- Risk factors, Obesity in children -- Diagnosis, Obesity in children -- Care and treatment, Obesity in children -- Research
Abstract

Maternal obesity is thought to increase the offspring's risk of juvenile obesity and metabolic diseases; however, the mechanism(s) whereby excess maternal nutrition affects fetal development remain poorly understood. Here, we investigated in nonhuman primates the effect of chronic high-fat diet (HFD) on the development of fetal metabolic systems. We found that fetal offspring from both lean and obese mothers chronically consuming a HFD had a 3-fold increase in liver triglycerides (TGs). In addition, fetal offspring from HFD-fed mothers (O-HFD) showed increased evidence of hepatic oxidative stress early in the third trimester, consistent with the development of nonalcoholic fatty liver disease (NAFLD). O-HFD animals also exhibited elevated hepatic expression of gluconeogenic enzymes and transcription factors. Furthermore, fetal glycerol levels were 2-fold higher in O-HFD animals than in control fetal offspring and correlated with maternal levels. The increased fetal hepatic TG levels persisted at P180, concurrent with a 2-fold increase in percent body fat. Importantly, reversing the maternal HFD to a low-fat diet during a subsequent pregnancy improved fetal hepatic TG levels and partially normalized gluconeogenic enzyme expression, without changing maternal body weight. These results suggest that a developing fetus is highly vulnerable to excess lipids, independent of maternal diabetes and/or obesity, and that exposure to this may increase the risk of pediatric NAFLD., Introduction The prevalence of childhood obesity has increased dramatically in the United States over the past several decades. According to the most recent National Health and Nutrition Examination Survey (NHANES) [...]

Published
2009

29. High-throughput and high-efficiency sample preparation for single-cell proteomics using a nested nanowell chip

Author

Woo, Jongmin, primary, Williams, Sarah M., additional, Aguilera-Vazquez, Victor, additional, Sontag, Ryan L., additional, Moore, Ronald J., additional, Markillie, Lye Meng, additional, Mehta, Hardeep S., additional, Cantlon, Joshua, additional, Adkins, Joshua N., additional, Smith, Richard D., additional, Clair, Geremy C., additional, Pasa-Tolic, Ljiljana, additional, and Zhu, Ying, additional

Published
2021
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31. MicroPOTS Analysis of Barrett’s Esophageal Cell Line Models Identifies Proteomic Changes after Physiologic and Radiation Stress

Author

Weke, Kenneth, primary, Singh, Ashita, additional, Uwugiaren, Naomi, additional, Alfaro, Javier A., additional, Wang, Tongjie, additional, Hupp, Ted R., additional, O’Neill, J. Robert, additional, Vojtesek, Borek, additional, Goodlett, David R., additional, Williams, Sarah M., additional, Zhou, Mowei, additional, Kelly, Ryan T., additional, Zhu, Ying, additional, and Dapic, Irena, additional

Published
2021
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33. Automated Coupling of Nanodroplet Sample Preparation with Liquid Chromatography–Mass Spectrometry for High-Throughput Single-Cell Proteomics

Author

Williams, Sarah M., primary, Liyu, Andrey V., additional, Tsai, Chia-Feng, additional, Moore, Ronald J., additional, Orton, Daniel J., additional, Chrisler, William B., additional, Gaffrey, Matthew J., additional, Liu, Tao, additional, Smith, Richard D., additional, Kelly, Ryan T., additional, Pasa-Tolic, Ljiljana, additional, and Zhu, Ying, additional

Published
2020
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38. Autism-associated miR-873 regulates ARID1B, SHANK3 and NRXN2 involved in neurodevelopment

Author

Lu, Jing, Zhu, Yan, Williams, Sarah M., Watts, Michelle E, Tonta, Mary A, Coleman, Harold, Parkington, Helena, Claudianos, Charles, Lu, Jing, Zhu, Yan, Williams, Sarah M., Watts, Michelle E, Tonta, Mary A, Coleman, Harold, Parkington, Helena, and Claudianos, Charles

Abstract

Autism spectrum disorders (ASD) are highly heritable neurodevelopmental disorders with significant genetic heterogeneity. Noncoding microRNAs (miRNAs) are recognised as playing key roles in development of ASD albeit the function of these regulatory genes remains unclear. We previously conducted whole-exome sequencing of Australian families with ASD and identified four novel single nucleotide variations in mature miRNA sequences. A pull-down transcriptome analysis using transfected SH-SY5Y cells proposed a mechanistic model to examine changes in binding affinity associated with a unique mutation found in the conserved 'seed' region of miR-873-5p (rs777143952: T > A). Results suggested several ASD-risk genes were differentially targeted by wild-type and mutant miR-873 variants. In the current study, a dual-luciferase reporter assay confirmed miR-873 variants have a 20-30% inhibition/dysregulation effect on candidate autism risk genes ARID1B, SHANK3 and NRXN2 and also confirmed the affected expression with qPCR. In vitro mouse hippocampal neurons transfected with mutant miR-873 showed less morphological complexity and enhanced sodium currents and excitatory neurotransmission compared to cells transfected with wild-type miR-873. A second in vitro study showed CRISPR/Cas9 miR-873 disrupted SH-SY5Y neuroblastoma cells acquired a neuronal-like morphology and increased expression of ASD important genes ARID1B, SHANK3, ADNP2, ANK2 and CHD8. These results represent the first functional evidence that miR-873 regulates key neural genes involved in development and cell differentiation.

Published
2020

40. Evaluation of scaffolding, inflammatory response, and wound healing support of a reverse thermal gel for myelomeningocele patching.

Author

Bardill, James R., Williams, Sarah M., Laughter, Melissa R., Park, Daewon, and Marwan, Ahmed I.

Subjects
INFLAMMATION, MYELOMENINGOCELE, HEALING, WOUND healing
Abstract

A reverse thermal gel (RTG) is a promising patching material for in utero, minimally invasive coverage of myelomeningocele (MMC) defects. The injectable properties of the RTG brings the potential for significantly reduced surgical risks to the mother and fetus when compared to current open prenatal repair procedures. MMC patching materials require structural and wound healing support for tissue growth over the MMC defect area to allow a watertight seal to form and prevent further neural tissue exposure to the amniotic environment. Here, the previously described RTG is evaluated for the first time as a scaffold for skin cells, for long‐term inflammation effects in neonatal mice, and for wound healing capability. Results show that the RTG can support the growth and survival of keratinocytes, dermal fibroblasts, and neuronal cells in vitro. Injections into neonatal mice demonstrate a regressing inflammatory response and support of normal wound healing. Together, these results demonstrate that the RTG has the necessary scaffolding and wound healing support necessary for MMC patching applications. [ABSTRACT FROM AUTHOR]

Published
2021
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43. Hypoxia-Induced MicroRNA-210 Targets Neurodegenerative Pathways

Author

Watts, Michelle E., Williams, Sarah M., Nithianantharajah, Jess, Claudianos, Charles, Watts, Michelle E., Williams, Sarah M., Nithianantharajah, Jess, and Claudianos, Charles

Abstract

Hypoxia-regulated microRNA-210 (miR-210) is a highly conserved microRNA, known to regulate various processes under hypoxic conditions. Previously we found that miR-210 is also involved in honeybee learning and memory, raising the questions of how neural activity may induce hypoxia-regulated genes and how miR-210 may regulate plasticity in more complex mammalian systems. Using a pull-down approach, we identified 620 unique target genes of miR-210 in humans, among which there was a significant enrichment of age-related neurodegenerative pathways, including Huntington’s, Alzheimer’s, and Parkinson’s diseases. We have also validated that miR-210 directly regulates various identified target genes of interest involved with neuronal plasticity, neurodegenerative diseases, and miR-210-associated cancers. This data suggests a potentially novel mechanism for how metabolic changes may couple plasticity to neuronal activity through hypoxia-regulated genes such as miR-210.

Published
2018

44. An integrative analysis of non-coding regulatory DNA variations associated with autism spectrum disorder

Author

Williams, Sarah M, An, Joon Yong, Edson, Janette, Watts, Michelle E, Murigneux, Valentine, Whitehouse, Andrew J.O, Jackson, Colin, Bellgrove, Mark, Cristino, Alexandre S, Claudianos, Charles, Williams, Sarah M, An, Joon Yong, Edson, Janette, Watts, Michelle E, Murigneux, Valentine, Whitehouse, Andrew J.O, Jackson, Colin, Bellgrove, Mark, Cristino, Alexandre S, and Claudianos, Charles

Abstract

A number of genetic studies have identified rare protein-coding DNA variations associated with autism spectrum disorder (ASD), a neurodevelopmental disorder with significant genetic etiology and heterogeneity. In contrast, the contributions of functional, regulatory genetic variations that occur in the extensive non-protein-coding regions of the genome remain poorly understood. Here we developed a genome-wide analysis to identify the rare single nucleotide variants (SNVs) that occur in non-coding regions and determined the regulatory function and evolutionary conservation of these variants. Using publicly available datasets and computational predictions, we identified SNVs within putative regulatory regions in promoters, transcription factor binding sites, and microRNA genes and their target sites. Overall, we found that the regulatory variants in ASD cases were enriched in ASD-risk genes and genes involved in fetal neurodevelopment. As with previously reported coding mutations, we found an enrichment of the regulatory variants associated with dysregulation of neurodevelopmental and synaptic signaling pathways. Among these were several rare inherited SNVs found in the mature sequence of microRNAs predicted to affect the regulation of ASD-risk genes. We show a paternally inherited miR-873-5p variant with altered binding affinity for several risk-genes including NRXN2 and CNTNAP2 putatively overlay maternally inherited lossof- function coding variations in NRXN1 and CNTNAP2 to likely increase the genetic liability in an idiopathic ASD case. Our analysis pipeline provides a new resource for identifying loss-of-function regulatory DNA variations that may contribute to the genetic etiology of complex disorders.

Published
2018

45. Comprehensive characterization of distinct states of human naive pluripotency generated by reprogramming

Author

Liu, Xiaodong, primary, Nefzger, Christian M, additional, Rossello, Fernando J, additional, Chen, Joseph, additional, Knaupp, Anja S, additional, Firas, Jaber, additional, Ford, Ethan, additional, Pflueger, Jahnvi, additional, Paynter, Jacob M, additional, Chy, Hun S, additional, O'Brien, Carmel M, additional, Huang, Cheng, additional, Mishra, Ketan, additional, Hodgson-Garms, Margeaux, additional, Jansz, Natasha, additional, Williams, Sarah M, additional, Blewitt, Marnie E, additional, Nilsson, Susan K, additional, Schittenhelm, Ralf B, additional, Laslett, Andrew L, additional, Lister, Ryan, additional, and Polo, Jose M, additional

Published
2017
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46. A Survey of Mississippi Beef Cattle Producer Attitudes, Practices, and Demographics.

Author

Montgomery-Williams, Sarah M., Brumbelow, Kaitlin, Larson, Jamie E., Maples, Josh, and Karisch, Brandi B.

Subjects
*BEEF industry, *BEEF cattle, *HEIFERS, *CATTLE, *BEEF quality, *INCOME, *SPECIAL sales
Abstract

As input costs increase, producers need to be mindful of management practices to maintain profit margins and it is important to understand current management practices. Therefore, the objective of this study was to investigate current beef marketing strategies and beliefs of beef producers in the state of Mississippi in 2019. This survey was distributed to cattle producers in Mississippi in the June/July issue of "Cattle Business in Mississippi" magazine with return postage. There also was a link included in the "Monday Memo" email sent to members of the Mississippi Cattlemen's Association. The survey consisted of 22 questions that were divided into three sections: current practices, current cow-calf marketing practice, and general information. Responses from the survey were anonymous and confidential and were received via paper mail or electronic responses. Responses were stored and analyzed using Qualtrics. Data collected from this study were compared with 1999 data from a similar study conducted by Little et al. (2000). Out of 148 respondents, there was a 95% completion rate of surveys taken. Most respondents were 51 years and older with 54% of the respondents being part of the cattle industry for over 31 years. Ninety percent of respondents were members of the Mississippi Cattlemen's Association and almost 60% were certified in Beef Quality Assurance. The majority, 122 of 148 producers, stated their cattle operation was not the primary source of income for their household. The average number of cows, bulls, stockers/yearling, replacement heifers and cattle on-feed on an operation was greater in the 2019 data compared with 1999. On average, the number of cows per operation increased from 40 to 68 animals, bulls increased from 2 to 5 animals, and replacement heifers increased from 7 to 17 animals from 1999 to 2019. There was also an average increase from 30 to76 animals of stocker/yearling and an increase from 2 to 27 animals of on-feed cattle. Most producers vaccinate (81%) and deworm (85%) according to recommendations and indicated a lack of labor and time as reasons for not implementing some common management practices such as preconditioning. Respondents mainly purchased calves directly from a producer (61%) or from special sales (59%). In 1999, over one-half of respondents purchased from an auction. When it came to selling cattle, 58% of respondents sold at auction regularly in 2019. In 1999, 73% of respondents sold at auctions. In 2019, 72% of respondents stated they did not retain ownership while in 1999 only 58% of respondents did not retain ownership. In conclusion, our results suggest there have been key changes within the cattle industry regarding herd size increases and a shift in selling and purchasing habits since 1999. [ABSTRACT FROM AUTHOR]

Published
2023
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48. Identification of the genomic mutation inEpha4rb-2J/rb-2Jmice

Author

Mohd-Zin, Siti W., primary, Abdullah, Nor-Linda, additional, Abdullah, Aminah, additional, Greene, Nicholas D.E., additional, Cheah, Pike-See, additional, Ling, King-Hwa, additional, Yusof, Hadri, additional, Marwan, Ahmed I., additional, Williams, Sarah M., additional, York, Kerri T., additional, Ahmad-Annuar, Azlina, additional, and Abdul-Aziz, Noraishah M., additional

Published
2016
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50. HDAC6 contributes to pathological responses of heart and skeletal muscle to chronic angiotensin-II signaling

Author

Demos-Davies, Kimberly M., primary, Ferguson, Bradley S., additional, Cavasin, Maria A., additional, Mahaffey, Jennifer H., additional, Williams, Sarah M., additional, Spiltoir, Jessica I., additional, Schuetze, Katherine B., additional, Horn, Todd R., additional, Chen, Bo, additional, Ferrara, Claudia, additional, Scellini, Beatrice, additional, Piroddi, Nicoletta, additional, Tesi, Chiara, additional, Poggesi, Corrado, additional, Jeong, Mark Y., additional, and McKinsey, Timothy A., additional

Published
2014
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