Principal Investigator

I Jonathan
Amster
Awardee Organization

University Of Georgia
United States

Fiscal Year
2020
Activity Code
U01
Project End Date

An Automated Platform for the CE-MS Analysis of Glycosaminoglycans

This project will develop an automated capillary electrophoresis-­tandem mass spectrometry platform for the  structural analysis of mixtures of glycosaminoglycan oligomers that are isolated in protein binding assays. This  class of carbohydrates can be found on the surface of all animal cells, and play a key role in many important  biological processes. Glycosaminoglycans are linear, polysulfated copolymers, typically with a repeating  disaccharide unit composed of an N-­acetyl-­hexosamine and glucuronic acid, and can be more than 200 repeat  units long. Modifications can occur anywhere along the chain, and these include O-­sulfation, N-­ deacetylation/N-­sulfation, and epimerization of the uronic acid. These are a particularly challenging class of  compounds to characterize due to their heterogeneous structures, an outcome of their non-­template  biosynthesis. Nevertheless, within the long glycan chains are short regions of defined modification that target  specific proteins with remarkable specificity. These glycan-­protein interactions are the basis for the biological  activity of the glycosaminoglycan. There is a critical need for tools to find these organized regions with the long  glycan chain, and to determine their pattern of modification. A few specialized laboratories have developed  mass spectrometry methods for the structural analysis of glycosaminoglycans, but these have not found their  way into biological laboratories at large. The goal of this project is to produce a platform with a high degree of  automation so that it can be deployed in the laboratories of biology researchers. The accessibility of these  advanced mass spectrometry methods will result from innovations in hardware, software, and methods  development.

Publications

  • Uhl FE, Zhang F, Pouliot RA, Uriarte JJ, Rolandsson Enes S, Han X, Ouyang Y, Xia K, Westergren-Thorsson G, Malmström A, Hallgren O, Linhardt RJ, Weiss DJ. Functional role of glycosaminoglycans in decellularized lung extracellular matrix. Acta biomaterialia. 2020 Jan 15;102:231-246. Epub 2019 Nov 18. PMID: 31751810
  • Kim SY, Zhang F, Harris DA, Linhardt RJ. Structural Features of Heparin and Its Interactions With Cellular Prion Protein Measured by Surface Plasmon Resonance. Frontiers in molecular biosciences. 2020 Nov 26;7:594497. doi: 10.3389/fmolb.2020.594497. eCollection 2020. PMID: 33324681
  • Datta P, Fu L, He W, Koffas MAG, Dordick JS, Linhardt RJ. Expression of enzymes for 3'-phosphoadenosine-5'-phosphosulfate (PAPS) biosynthesis and their preparation for PAPS synthesis and regeneration. Applied microbiology and biotechnology. 2020 Aug;104(16):7067-7078. Epub 2020 Jun 29. PMID: 32601738
  • Kim SY, Jin W, Sood A, Montgomery DW, Grant OC, Fuster MM, Fu L, Dordick JS, Woods RJ, Zhang F, Linhardt RJ. Characterization of heparin and severe acute respiratory syndrome-related coronavirus 2 (SARS-CoV-2) spike glycoprotein binding interactions. Antiviral research. 2020 Sep;181:104873. Epub 2020 Jul 10. PMID: 32653452
  • Yan L, Song Y, Xia K, He P, Zhang F, Chen S, Pouliot R, Weiss DJ, Tandon R, Bates JT, Ederer DR, Mitra D, Sharma P, Davis A, Linhardt RJ. Heparan sulfates from bat and human lung and their binding to the spike protein of SARS-CoV-2 virus. Carbohydrate polymers. 2021 May 15;260:117797. Epub 2021 Feb 14. PMID: 33712145
  • Lin L, Li B, Han X, Zhang F, Zhang X, Linhardt RJ. A rolling circle amplification based platform for ultrasensitive detection of heparin. The Analyst. 2021 Jan 21;146(2):714-720. Epub 2020 Nov 23. PMID: 33226386
  • Qiao M, Li B, Ji Y, Lin L, Linhardt R, Zhang X. Synthesis of selected unnatural sugar nucleotides for biotechnological applications. Critical reviews in biotechnology. 2021 Feb;41(1):47-62. Epub 2020 Nov 5. PMID: 33153306
  • Kim SY, Kundu J, Williams A, Yandulskaya AS, Monaghan JR, Carrier RL, Linhardt RJ. Glycosaminoglycans compositional analysis of Urodele axolotl (Ambystoma mexicanum) and Porcine Retina. Glycoconjugate journal. 2019 Apr;36(2):165-174. Epub 2019 Apr 8. PMID: 30963354
  • Pepi LE, Leach FE 3rd, Klein DR, Brodbelt JS, Amster IJ. Investigation of the Experimental Parameters of Ultraviolet Photodissociation for the Structural Characterization of Chondroitin Sulfate Glycosaminoglycan Isomers. Journal of the American Society for Mass Spectrometry. 2021 Jul 7;32(7):1759-1770. Epub 2021 Jun 6. PMID: 34096288
  • Lin L, Yu Y, Zhang F, Xia K, Zhang X, Linhardt RJ. Bottom-up and top-down profiling of pentosan polysulfate. The Analyst. 2019 Aug 5;144(16):4781-4786. PMID: 31287456
  • Weiner SA, Aristizabal S, Alberts DS, Surwit EA, Deatherage-Deuser K. A phase II trial of mitomycin, vincristine, bleomycin, and cisplatin (MOBP) as neoadjuvant therapy in high-risk cervical carcinoma. Gynecologic oncology. 1988 May;30(1):1-6. PMID: 2452769
  • Yan L, Xia K, Yu Y, Miliakos A, Chaturvedi S, Zhang F, Chen S, Chaturvedi V, Linhardt RJ. Unique Cell Surface Mannan of Yeast Pathogen Candida auris with Selective Binding to IgG. ACS infectious diseases. 2020 May 8;6(5):1018-1031. Epub 2020 Apr 10. PMID: 32233507
  • Stickney M, Xia Q, Amster IJ. Investigation of electrospray for a capillary electrophoresis-mass spectrometry interface in reverse polarity and negative ion mode. European journal of mass spectrometry (Chichester, England). 2019 Feb;25(1):157-163. PMID: 30773923
  • Duan J, Jonathan Amster I. An Automated, High-Throughput Method for Interpreting the Tandem Mass Spectra of Glycosaminoglycans. Journal of the American Society for Mass Spectrometry. 2018 Sep;29(9):1802-1811. Epub 2018 May 22. PMID: 29790112
  • Kim SY, Koetzner CA, Payne AF, Nierode GJ, Yu Y, Wang R, Barr E, Dordick JS, Kramer LD, Zhang F, Linhardt RJ. Glycosaminoglycan Compositional Analysis of Relevant Tissues in Zika Virus Pathogenesis and in Vitro Evaluation of Heparin as an Antiviral against Zika Virus Infection. Biochemistry. 2019 Feb 26;58(8):1155-1166. Epub 2019 Feb 13. PMID: 30698412
  • Cress BF, Bhaskar U, Vaidyanathan D, Williams A, Cai C, Liu X, Fu L, M-Chari V, Zhang F, Mousa SA, Dordick JS, Koffas MAG, Linhardt RJ. Heavy Heparin: A Stable Isotope-Enriched, Chemoenzymatically-Synthesized, Poly-Component Drug. Angewandte Chemie (International ed. in English). 2019 Apr 23;58(18):5962-5966. Epub 2019 Apr 1. PMID: 30870573
  • Pepi LE, Sasiene ZJ, Mendis PM, Jackson GP, Amster IJ. Structural Characterization of Sulfated Glycosaminoglycans Using Charge-Transfer Dissociation. Journal of the American Society for Mass Spectrometry. 2020 Oct 7;31(10):2143-2153. Epub 2020 Sep 3. PMID: 32820910
  • Pepi LE, Amster IJ. Electron-Activated Tandem Mass Spectrometry Analysis of Glycosaminoglycans. Current protocols. 2021 Apr;1(4):e83. PMID: 33798269
  • Clark GT, Yu Y, Urban CA, Fu G, Wang C, Zhang F, Linhardt RJ, Hurley JM. Circadian control of heparan sulfate levels times phagocytosis of amyloid beta aggregates. PLoS genetics. 2022 Feb 10;18(2):e1009994. doi: 10.1371/journal.pgen.1009994. eCollection 2022 Feb. PMID: 35143487
  • Vaidyanathan D, Paskaleva E, Vargason T, Ke X, McCallum SA, Linhardt RJ, Dordick JS. Elucidating the unusual reaction kinetics of D-glucuronyl C5-epimerase. Glycobiology. 2020 Oct 21;30(11):847-858. PMID: 32304324
  • Yu Y, Zhang F, Renois-Predelus G, Amster IJ, Linhardt RJ. Filter-entrapment enrichment pull-down assay for glycosaminoglycan structural characterization and protein interaction. Carbohydrate polymers. 2020 Oct 1;245:116623. Epub 2020 Jun 10. PMID: 32718661
  • Datta P, Yan L, Awofiranye A, Dordick JS, Linhardt RJ. Heparosan Chain Characterization: Sequential Depolymerization of E. Coli K5 Heparosan by a Bacterial Eliminase Heparin Lyase III and a Bacterial Hydrolase Heparanase Bp to Prepare Defined Oligomers. Biotechnology journal. 2021 Mar;16(3):e2000336. Epub 2020 Nov 10. PMID: 33006278
  • Song Y, Zhang F, Linhardt RJ. Analysis of the Glycosaminoglycan Chains of Proteoglycans. The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society. 2021 Feb;69(2):121-135. Epub 2020 Jul 6. PMID: 32623943
  • Yu Y, Bruzdoski K, Kostousov V, Hensch L, Hui SK, Siddiqui F, Farooqui A, Kouta A, Zhang F, Fareed J, Teruya J, Linhardt RJ. Structural characterization of a clinically described heparin-like substance in plasma causing bleeding. Carbohydrate polymers. 2020 Sep 15;244:116443. Epub 2020 May 19. PMID: 32536393
  • Jin W, Jiang D, Zhang W, Wang C, Xia K, Zhang F, Linhardt RJ. Interactions of fibroblast growth factors with sulfated galactofucan from Saccharina japonica. International journal of biological macromolecules. 2020 Oct 1;160:26-34. Epub 2020 May 25. PMID: 32464202
  • Zhang F, Zhao J, Liu X, Linhardt RJ. Interactions between Sclerostin and Glycosaminoglycans. Glycoconjugate journal. 2020 Feb;37(1):119-128. Epub 2019 Dec 11. PMID: 31828567
  • Lin L, Yu Y, Zhang F, Zhang X, Linhardt RJ. High-throughput method for in process monitoring of 3-O-sulfotransferase catalyzed sulfonation in bioengineered heparin synthesis. Analytical biochemistry. 2019 Dec 1;586:113419. Epub 2019 Sep 10. PMID: 31518551
  • Duan J, Pepi L, Amster IJ. A Scoring Algorithm for the Automated Analysis of Glycosaminoglycan MS/MS Data. Journal of the American Society for Mass Spectrometry. 2019 Dec;30(12):2692-2703. Epub 2019 Oct 31. PMID: 31673949
  • Pomin VH, Mahdi F, Jin W, Zhang F, Linhardt RJ, Paris JJ. Red Algal Sulfated Galactan Binds and Protects Neural Cells from HIV-1 gp120 and Tat. Pharmaceuticals (Basel, Switzerland). 2021 Jul 23;14. (8). PMID: 34451811
  • Baytas SN, Linhardt RJ. Advances in the preparation and synthesis of heparin and related products. Drug discovery today. 2020 Dec;25(12):2095-2109. Epub 2020 Sep 16. PMID: 32947045
  • Yan L, Brodfueher P, Fu L, Zhang F, Chen S, Dordick JS, Linhardt RJ. Chemical O-sulfation of N-sulfoheparosan: a route to rare N-sulfo-3-O-sulfoglucosamine and 2-O-sulfoglucuronic acid. Glycoconjugate journal. 2020 Oct;37(5):589-597. Epub 2020 Aug 10. PMID: 32778986
  • Jin W, Zhang W, Mitra D, McCandless MG, Sharma P, Tandon R, Zhang F, Linhardt RJ. The structure-activity relationship of the interactions of SARS-CoV-2 spike glycoproteins with glucuronomannan and sulfated galactofucan from Saccharina japonica. International journal of biological macromolecules. 2020 Nov 15;163:1649-1658. Epub 2020 Sep 24. PMID: 32979436
  • Datta P, Fu L, Brodfuerer P, Dordick JS, Linhardt RJ. High density fermentation of probiotic E. coli Nissle 1917 towards heparosan production, characterization, and modification. Applied microbiology and biotechnology. 2021 Feb;105(3):1051-1062. Epub 2021 Jan 22. PMID: 33481068
  • Zhang F, Zheng L, Cheng S, Peng Y, Fu L, Zhang X, Linhardt RJ. Comparison of the Interactions of Different Growth Factors and Glycosaminoglycans. Molecules (Basel, Switzerland). 2019 Sep 16;24. (18). PMID: 31527407
  • Stickney M, Sanderson P, Leach FE 3rd, Zhang F, Linhardt RJ, Amster IJ. Online Capillary Zone Electrophoresis Negative Electron Transfer Dissociation Tandem Mass Spectrometry of Glycosaminoglycan Mixtures. International journal of mass spectrometry. 2019 Nov;445. Epub 2019 Aug 17. PMID: 32641905
  • Yan L, Fu L, Xia K, Chen S, Zhang F, Dordick JS, Linhardt RJ. A Revised Structure for the Glycolipid Terminus of Escherichia coli K5 Heparosan Capsular Polysaccharide. Biomolecules. 2020 Nov 6;10. (11). PMID: 33171953
  • Zhang X, Han X, Xia K, Xu Y, Yang Y, Oshima K, Haeger SM, Perez MJ, McMurtry SA, Hippensteel JA, Ford JA, Herson PS, Liu J, Schmidt EP, Linhardt RJ. Circulating heparin oligosaccharides rapidly target the hippocampus in sepsis, potentially impacting cognitive functions. Proceedings of the National Academy of Sciences of the United States of America. 2019 May 7;116(19):9208-9213. Epub 2019 Apr 22. PMID: 31010931
  • Xia K, Hagan JT, Fu L, Sheetz BS, Bhattacharya S, Zhang F, Dwyer JR, Linhardt RJ. Synthetic heparan sulfate standards and machine learning facilitate the development of solid-state nanopore analysis. Proceedings of the National Academy of Sciences of the United States of America. 2021 Mar 16;118. (11). PMID: 33688052
  • Klein DR, Leach FE 3rd, Amster IJ, Brodbelt JS. Structural Characterization of Glycosaminoglycan Carbohydrates Using Ultraviolet Photodissociation. Analytical chemistry. 2019 May 7;91(9):6019-6026. Epub 2019 Apr 11. PMID: 30932467
  • Sanderson P, Stickney M, Leach FE 3rd, Xia Q, Yu Y, Zhang F, Linhardt RJ, Amster IJ. Heparin/heparan sulfate analysis by covalently modified reverse polarity capillary zone electrophoresis-mass spectrometry. Journal of chromatography. A. 2018 Apr 13;1545:75-83. Epub 2018 Feb 24. PMID: 29501428
  • Bhattacharyya S, Feferman L, Han X, Xia K, Zhang F, Linhardt RJ, Tobacman JK. Increased CHST15 follows decline in arylsulfatase B (ARSB) and disinhibition of non-canonical WNT signaling: potential impact on epithelial and mesenchymal identity. Oncotarget. 2020 Jun 16;11(24):2327-2344. doi: 10.18632/oncotarget.27634. eCollection 2020 Jun 16. PMID: 32595831
  • Qiao M, Lin L, Xia K, Li J, Zhang X, Linhardt RJ. Recent advances in biotechnology for heparin and heparan sulfate analysis. Talanta. 2020 Nov 1;219:121270. Epub 2020 Jun 14. PMID: 32887160
  • Pepi LE, Sanderson P, Stickney M, Amster IJ. Developments in Mass Spectrometry for Glycosaminoglycan Analysis: A Review. Molecular & cellular proteomics : MCP. 2021;20:100025. Epub 2021 Jan 6. PMID: 32938749
  • Jin W, Zhang F, Linhardt RJ. Bioengineered production of glycosaminoglycans and their analogues. Systems microbiology and biomanufacturing. 2021 Apr;1(2):123-130. Epub 2020 Aug 17. PMID: 38524245