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Herein, an on-tissue chemical derivatization strategy based on positively charged hydrazine reagent (Girard\u2019s reagent P) coupled with matrix-assisted laser desorption\/ionization mass spectrometry imaging (MALDI-MSI) was developed for analysis of N-glycans from FFPE treated tissue sections. The performance of the proposed approach was evaluated by analysis of monosaccharides, oligosaccharides, N-glycans released from glycoproteins, as well as MS imaging of N-glycans from human cancer tissue sections. The results demonstrated that the signal-to-noise ratios for target saccharides were notably improved after chemical derivatization, in which signals were enhanced by 230-fold for glucose and over 28-fold for maltooctaose. Improved glycome coverage was obtained for N-glycans derived from glycoproteins and tissue samples after chemical derivatization. Furthermore, on-tissue derivatization was applied for MALDI-MSI of N-glycans from human laryngeal cancer and ovarian cancer tissues. Differentially expressed N-glycans among the tumor region, adjacent normal tissue region, and tumor proximal collagen stroma region were imaged, revealing that high-mannose type N-glycans were predominantly expressed in the tumor region. Overall, our results indicate that the on-tissue labeling strategy coupled with MALDI-MSI shows great potential to spatially characterize N-glycan expression within heterogeneous tissue samples with enhanced sensitivity. This study provides a promising approach to better understand the pathogenesis of cancer related aberrant glycosylation, which is beneficial to the design of improved clinical diagnosis and therapeutic strategies.<\/jats:p>","DOI":"10.1021\/acs.analchem.0c02704","type":"journal-article","created":{"date-parts":[[2020,8,31]],"date-time":"2020-08-31T14:19:20Z","timestamp":1598883560000},"page":"13361-13368","source":"Crossref","is-referenced-by-count":71,"title":["On-Tissue Derivatization with Girard\u2019s Reagent\nP Enhances N-Glycan Signals for Formalin-Fixed Paraffin-Embedded\nTissue Sections in MALDI Mass Spectrometry Imaging"],"prefix":"10.1021","volume":"92","author":[{"given":"Hua","family":"Zhang","sequence":"first","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xudong","family":"Shi","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53792"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nhu Q.","family":"Vu","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2367-4433","authenticated-orcid":true,"given":"Gongyu","family":"Li","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zihui","family":"Li","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yatao","family":"Shi","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miyang","family":"Li","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bin","family":"Wang","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nathan V.","family":"Welham","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53792"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manish S.","family":"Patankar","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 54911"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Weisman","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53792"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0056-3869","authenticated-orcid":true,"given":"Lingjun","family":"Li","sequence":"additional","affiliation":[{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]},{"name":"University of Wisconsin\u2500Madison , , , ,","place":["Madison, Wisconsin, United States, 53705"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,8,31]]},"reference":[{"key":"2026090203044339700_cit1","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1016\/j.cell.2010.11.008","article-title":"Glycomics\nhits the big time","volume":"143","author":"Hart","year":"2010","journal-title":"Cell"},{"key":"2026090203044339700_cit2","doi-asserted-by":"publisher","first-page":"448","DOI":"10.1038\/nrm3383","article-title":"Vertebrate\nprotein glycosylation:\ndiversity, synthesis and function","volume":"13","author":"Moremen","year":"2012","journal-title":"Nat. Rev.\nMol. Cell Biol."},{"key":"2026090203044339700_cit3","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1093\/glycob\/cww086","article-title":"Biological\nroles of glycans","volume":"27","author":"Varki","year":"2017","journal-title":"Glycobiology"},{"key":"2026090203044339700_cit4","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1038\/nrc3982","article-title":"Glycosylation in\ncancer: mechanisms and clinical implications","volume":"15","author":"Pinho","year":"2015","journal-title":"Nat. Rev. Cancer"},{"key":"2026090203044339700_cit5","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1007\/s00216-016-9880-6","article-title":"Glycans and glycoproteins as specific\nbiomarkers for cancer","volume":"409","author":"Kailemia","year":"2017","journal-title":"Anal. Bioanal. Chem."},{"key":"2026090203044339700_cit6","doi-asserted-by":"publisher","first-page":"918","DOI":"10.1016\/j.cell.2010.02.016","article-title":"Mechanisms underlying inflammation\nin neurodegeneration","volume":"140","author":"Glass","year":"2010","journal-title":"Cell"},{"key":"2026090203044339700_cit7","doi-asserted-by":"publisher","first-page":"6050","DOI":"10.1073\/pnas.1424017112","article-title":"Diabetes-associated\ndysregulation of O-GlcNAcylation\nin rat cardiac mitochondria","volume":"112","author":"Banerjee","year":"2015","journal-title":"Proc. Natl. Acad.\nSci. U. S. 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Chem."},{"key":"2026090203044339700_cit26","doi-asserted-by":"publisher","first-page":"12942","DOI":"10.1021\/acs.analchem.9b02995","article-title":"Mass Spectrometry\nImaging of N-Glycans\nfrom Formalin-Fixed Paraffin-Embedded Tissue Sections Using a Novel\nSubatmospheric Pressure Ionization Source","volume":"91","author":"Shi","year":"2019","journal-title":"Anal.\nChem."},{"key":"2026090203044339700_cit27","doi-asserted-by":"publisher","first-page":"3457","DOI":"10.1007\/s00216-010-3532-z","article-title":"Glycan labeling strategies and their use in identification\nand quantification","volume":"397","author":"Ruhaak","year":"2010","journal-title":"Anal. Bioanal. Chem."},{"key":"2026090203044339700_cit28","doi-asserted-by":"publisher","first-page":"1196","DOI":"10.1016\/j.jchromb.2010.11.010","article-title":"Derivatization\nof carbohydrates for analysis by chromatography; electrophoresis and\nmass spectrometry","volume":"879","author":"Harvey","year":"2011","journal-title":"J. Chromatogr. B: Anal. Technol.\nBiomed. Life Sci."},{"key":"2026090203044339700_cit29","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1016\/0008-6215(84)85242-8","article-title":"A simple and rapid method for the\npermethylation of carbohydrates","volume":"131","author":"Ciucanu","year":"1984","journal-title":"Carbohydr.\nRes."},{"key":"2026090203044339700_cit30","doi-asserted-by":"publisher","first-page":"6527","DOI":"10.1021\/acs.analchem.5b01835","article-title":"Capillary electrophoresis-electrospray ionization-mass spectrometry\nfor quantitative analysis of glycans labeled with multiplex carbonyl-reactive\ntandem mass tags","volume":"87","author":"Zhong","year":"2015","journal-title":"Anal. 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Chem."},{"key":"2026090203044339700_cit33","doi-asserted-by":"publisher","first-page":"7817","DOI":"10.1021\/acs.analchem.8b00548","article-title":"Quantitative glycomic\nanalysis by mass-defect-based dimethyl pyrimidinyl ornithine (DiPyrO)\ntags and high-resolution mass spectrometry","volume":"90","author":"Chen","year":"2018","journal-title":"Anal. 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Proteome Res."},{"key":"2026090203044339700_cit36","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1039\/B915589A","article-title":"Increasing the hydrophobicity and\nelectrospray response of glycans through derivatization with novel\ncationic hydrazides","volume":"46","author":"Bereman","year":"2010","journal-title":"Chem. Commun."},{"key":"2026090203044339700_cit37","doi-asserted-by":"publisher","first-page":"6738","DOI":"10.1021\/ac201376q","article-title":"Stable-isotope labeled\nhydrophobic hydrazide reagents for the relative quantification of\nN-linked glycans by electrospray ionization mass spectrometry","volume":"83","author":"Walker","year":"2011","journal-title":"Anal. Chem."},{"key":"2026090203044339700_cit38","doi-asserted-by":"publisher","first-page":"8958","DOI":"10.1021\/acs.jafc.9b02635","article-title":"Matrix-assisted\nlaser desorption\/ionization time-of-flight mass spectrometry analysis\nof human milk neutral and sialylated free oligosaccharides using Girard\u2019s\nreagent P on-target derivatization","volume":"67","author":"Gao","year":"2019","journal-title":"J. Agric.\nFood Chem."},{"key":"2026090203044339700_cit39","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/j.aca.2018.10.015","article-title":"Sensitive and robust\nMALDI-TOF-MS glycomics analysis enabled by Girard\u2019s reagent\nT on-target derivatization (GTOD) of reducing glycans","volume":"1048","author":"Zhang","year":"2019","journal-title":"Anal. Chim. Acta"},{"key":"2026090203044339700_cit40","doi-asserted-by":"publisher","first-page":"366","DOI":"10.1002\/mas.21367","article-title":"The usefulness of hydrazine derivatives\nfor mass spectrometric\nanalysis of carbohydrates","volume":"32","author":"Lattova","year":"2013","journal-title":"Mass Spectrom. Rev."},{"key":"2026090203044339700_cit41","doi-asserted-by":"publisher","first-page":"5988","DOI":"10.1021\/acs.analchem.6b01021","article-title":"On-tissue\nderivatization via electrospray deposition for matrix assisted laser\ndesorption\/ionization mass spectrometry imaging of endogenous fatty\nacids in rat brain tissues","volume":"88","author":"Wu","year":"2016","journal-title":"Anal. 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Plant\nSci."},{"key":"2026090203044339700_cit44","doi-asserted-by":"publisher","first-page":"8918","DOI":"10.1021\/acs.analchem.9b00619","article-title":"Tandem mass\nspectrometry imaging reveals distinct accumulation patterns of steroid\nstructural isomers in human adrenal glands","volume":"91","author":"Takeo","year":"2019","journal-title":"Anal. Chem."},{"key":"2026090203044339700_cit45","doi-asserted-by":"publisher","first-page":"1431","DOI":"10.1021\/acs.analchem.9b04618","article-title":"Enhancement\nof on-tissue chemical derivatization by\nlaser-assisted tissue transfer for MALDI MS imaging","volume":"92","author":"Guo","year":"2020","journal-title":"Anal. Chem."},{"key":"2026090203044339700_cit46","doi-asserted-by":"publisher","first-page":"624","DOI":"10.1136\/bmj.39339.610000.BE","article-title":"The declaration of\nHelsinki","volume":"335","author":"Goodyear","year":"2007","journal-title":"Br. Med. 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Protoc."},{"key":"2026090203044339700_cit48","doi-asserted-by":"publisher","first-page":"1167","DOI":"10.1021\/pr401043r","article-title":"Filter-aided\nN-glycan separation (FANGS): A convenient sample preparation method\nfor mass spectrometric N-glycan profiling","volume":"13","author":"Rahman","year":"2014","journal-title":"J.\nProteome Res."},{"key":"2026090203044339700_cit49","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0106255","article-title":"MALDI imaging mass\nspectrometry profiling of N-glycans in formalin-fixed paraffin embedded\nclinical tissue blocks and tissue microarrays","volume":"9","author":"Powers","year":"2014","journal-title":"PLoS One"},{"key":"2026090203044339700_cit50","doi-asserted-by":"publisher","first-page":"3003","DOI":"10.1074\/mcp.M116.059816","article-title":"N-glycan MALDI imaging mass spectrometry\non formalin-fixed\nparaffin-embedded tissue enables the delineation of ovarian cancer\ntissues","volume":"15","author":"Everest-Dass","year":"2016","journal-title":"Mol. Cell. Proteomics"},{"key":"2026090203044339700_cit51","first-page":"59","article-title":"MALDI Mass\nSpectrometry Imaging of N-Linked Glycans in Tissues","volume-title":"Glycobiophysics","author":"Drake"},{"key":"2026090203044339700_cit52","doi-asserted-by":"publisher","first-page":"1650","DOI":"10.1021\/pr7008252","article-title":"GlycoWorkbench:\nA tool for the computer-assisted annotation\nof mass spectra of Glycans","volume":"7","author":"Ceroni","year":"2008","journal-title":"J. Proteome Res."},{"key":"2026090203044339700_cit53","doi-asserted-by":"publisher","first-page":"2137","DOI":"10.1038\/s41467-019-09910-7","article-title":"Highly sensitive CE-ESI-MS\nanalysis of N-glycans from complex biological samples","volume":"10","author":"Lageveen-Kammeijer","year":"2019","journal-title":"Nat. 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