Regioisomeric SCFA Attachment to Hexosamines Separates Metabolic Flux from Cytotoxicity and MUC1 Suppression (original) (raw)

ArticlesMarch 14, 2008

Regioisomeric SCFA Attachment to Hexosamines Separates Metabolic Flux from Cytotoxicity and MUC1 Suppression

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ACS Chemical Biology

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Abstract

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Chemical biology studies, exemplified by metabolic glycoengineering experiments that employ short chain fatty acid (SCFA)-hexosamine monosaccharide hybrid molecules, often suffer from off-target effects. Here we demonstrate that systematic structure–activity relationship (SAR) studies can deconvolute multiple biological activities of SCFA-hexosamine analogues by demonstrating that triacylated monosaccharides, including both _n_-butyrate- and acetate-modified ManNAc analogues, had dramatically different activities depending on whether the free hydroxyl group was at the C1 or C6 position. The C1-OH (hemiacetal) analogues enhanced growth inhibition in MDA-MB-231 human breast cancer cells and suppressed expression of MUC1, which are attractive properties for an anticancer agent. By contrast, C6-OH analogues supported high metabolic flux into the sialic acid pathway with negligible growth inhibition or toxicity, which are desirable properties for glycan labeling in healthy cells. Importantly, these SAR were general, applying to other hexosamines (e.g., GlcNAc) and non-natural sugar “scaffolds” (e.g., ManNLev). From a practical standpoint, the ability to separate toxicity from flux will facilitate the use of MOE analogues for cancer treatment and glycomics applications, respectively. Mechanistically, these findings overturn the premise that the bioactivities of SCFA-monosaccharide hybrid molecules result from their hydrolysis products (e.g., _n_-butyrate, which acts as a histone deacetylase inhibitor, and ManNAc, which activates sialic acid biosynthesis); instead the SAR establish that inherent properties of partially acylated hexosamines supersede the cellular responses supported by either the acyl or monosaccharide moieties.

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  1. Aleš Krčil, Lucia Šutvajová, Vojtěch Hamala, Ivana Císařová, Martin Kurfiřt, Lucie Červenková Št’astná, Jana Bernášková, Roman Hrstka, Jindřich Karban. Synthesis and Antiproliferative Activity of Fluorinated N-Acetylmannosamine Analogs. The Journal of Organic Chemistry 2026, 91 (13) , 4645-4656. https://doi.org/10.1021/acs.joc.5c03084
  2. Jiayu Sun, Zhimin Huang, Yifei Du, Pinou Lv, Xinqi Fan, Peng Dai, Xing Chen. Metabolic Glycan Labeling in Primary Neurons Enabled by Unnatural Sugars with No S-Glyco-Modification. ACS Chemical Biology 2023, 18 (6) , 1416-1424. https://doi.org/10.1021/acschembio.3c00152
  3. Christopher T. Saeui, Sagar R. Shah, Beatriz I. Fernandez-Gil, Cissy Zhang, Christian Agatemor, Kris Dammen-Brower, Mohit P. Mathew, Matthew Buettner, Prateek Gowda, Pratik Khare, Andrea Otamendi-Lopez, Shuang Yang, Hui Zhang, Anne Le, Alfredo Quinoñes-Hinojosa, Kevin J. Yarema. Anticancer Properties of Hexosamine Analogs Designed to Attenuate Metabolic Flux through the Hexosamine Biosynthetic Pathway. ACS Chemical Biology 2023, 18 (1) , 151-165. https://doi.org/10.1021/acschembio.2c00784
  4. Chiara Morozzi, Jana Sedláková, Michaela Serpi, Marialuce Avigliano, Rosangela Carbajo, Lucia Sandoval, Yadira Valles-Ayoub, Patrick Crutcher, Stephen Thomas, Fabrizio Pertusati. Targeting GNE Myopathy: A Dual Prodrug Approach for the Delivery of N-Acetylmannosamine 6-Phosphate. Journal of Medicinal Chemistry 2019, 62 (17) , 8178-8193. https://doi.org/10.1021/acs.jmedchem.9b00833
  5. Christopher T. Saeui, Lingshu Liu, Esteban Urias, Justin Morrissette-McAlmon, Rahul Bhattacharya, Kevin J. Yarema. Pharmacological, Physiochemical, and Drug-Relevant Biological Properties of Short Chain Fatty Acid Hexosamine Analogues Used in Metabolic Glycoengineering. Molecular Pharmaceutics 2018, 15 (3) , 705-720. https://doi.org/10.1021/acs.molpharmaceut.7b00525
  6. Balyn W. Zaro, Anna R. Batt, Kelly N. Chuh, Marisol X. Navarro, and Matthew R. Pratt . The Small Molecule 2-Azido-2-deoxy-glucose Is a Metabolic Chemical Reporter of O-GlcNAc Modifications in Mammalian Cells, Revealing an Unexpected Promiscuity of O-GlcNAc Transferase. ACS Chemical Biology 2017, 12 (3) , 787-794. https://doi.org/10.1021/acschembio.6b00877
  7. Thomas T. Zengeya, Rhushikesh A. Kulkarni, and Jordan L. Meier . Modular Synthesis of Cell-Permeating 2-Ketoglutarate Esters. Organic Letters 2015, 17 (10) , 2326-2329. https://doi.org/10.1021/acs.orglett.5b00737
  8. Albert M. DeBerardinis, Daniel J. Madden, Upasana Banerjee, Vibhavari Sail, Daniel S. Raccuia, Daniel De Carlo, Steven M. Lemieux, Adam Meares, and M. Kyle Hadden . Structure–Activity Relationships for Vitamin D3-Based Aromatic A-Ring Analogues as Hedgehog Pathway Inhibitors. Journal of Medicinal Chemistry 2014, 57 (9) , 3724-3736. https://doi.org/10.1021/jm401812d
  9. Jason C. Morris, Johanna Chiche, Caroline Grellier, Marie Lopez, Laurent F. Bornaghi, Alfonso Maresca, Claudiu T. Supuran, Jacques Pouysségur, and Sally-Ann Poulsen . Targeting Hypoxic Tumor Cell Viability with Carbohydrate-Based Carbonic Anhydrase IX and XII Inhibitors. Journal of Medicinal Chemistry 2011, 54 (19) , 6905-6918. https://doi.org/10.1021/jm200892s
  10. Marie Lopez, Jonathan Trajkovic, Laurent F. Bornaghi, Alessio Innocenti, Daniela Vullo, Claudiu T. Supuran, and Sally-Ann Poulsen . Design, Synthesis, and Biological Evaluation of Novel Carbohydrate-Based Sulfamates as Carbonic Anhydrase Inhibitors. Journal of Medicinal Chemistry 2011, 54 (5) , 1481-1489. https://doi.org/10.1021/jm101525j
  11. Yoshihiro Ueda, Wataru Muramatsu, Kenji Mishiro, Takumi Furuta and Takeo Kawabata. Functional Group Tolerance in Organocatalytic Regioselective Acylation of Carbohydrates. The Journal of Organic Chemistry 2009, 74 (22) , 8802-8805. https://doi.org/10.1021/jo901569v
  12. Marie Lopez, Blessy Paul, Andreas Hofmann, Julia Morizzi, Quoc K. Wu, Susan A. Charman, Alessio Innocenti, Daniela Vullo, Claudiu T. Supuran and Sally-Ann Poulsen . S-Glycosyl Primary Sulfonamides−A New Structural Class for Selective Inhibition of Cancer-Associated Carbonic Anhydrases. Journal of Medicinal Chemistry 2009, 52 (20) , 6421-6432. https://doi.org/10.1021/jm900914e
  13. Noha Elmouelhi, Udayanath Aich, Venkata D. P. Paruchuri, M. Adam Meledeo, Christopher T. Campbell, Jean J. Wang, Raja Srinivas, Hargun S. Khanna and Kevin J. Yarema. Hexosamine Template. A Platform for Modulating Gene Expression and for Sugar-Based Drug Discovery. Journal of Medicinal Chemistry 2009, 52 (8) , 2515-2530. https://doi.org/10.1021/jm801661m
  14. Christopher T. Campbell, Udayanath Aich, Christopher A. Weier, Jean J. Wang, Sean S. Choi, Mary M. Wen, Katharina Maisel, Srinivasa-Gopalan Sampathkumar and Kevin J. Yarema. Targeting Pro-Invasive Oncogenes with Short Chain Fatty Acid-Hexosamine Analogues Inhibits the Mobility of Metastatic MDA-MB-231 Breast Cancer Cells. Journal of Medicinal Chemistry 2008, 51 (24) , 8135-8147. https://doi.org/10.1021/jm800873k
  15. Luke D. Lavis. Ester Bonds in Prodrugs. ACS Chemical Biology 2008, 3 (4) , 203-206. https://doi.org/10.1021/cb800065s
  16. Maryam Musavi, Farnaz Oghbaei, Mohammad Abavisani, Ahmad Ghasemi, Amir Abbas Momtazi-Borojeni. The hexosamine biosynthesis pathway as a potent culprit in breast cancer progression. The Journal of Steroid Biochemistry and Molecular Biology 2026, 257 , 106932. https://doi.org/10.1016/j.jsbmb.2025.106932
  17. Kris Dammen-Brower, Stanley Zhu, Christian Agatemor, Safiya Aafreen, Vrinda Dharharma, Christopher T. Saeui, Hui Li, Jian Song, Matthew J. Buettner, Keith R. Kwagala, Hui Zhang, Howard E. Katz, Guanshu Liu, Kevin J. Yarema. Profiling the pancreatic cancer secretome with metabolic glycoengineering. Journal of Biological Chemistry 2026, 302 (3) , 111243. https://doi.org/10.1016/j.jbc.2026.111243
  18. Da-Yong Lu, Ting-Ren Lu. Sialic Acids and Cancer: Pathophysiological Association between Metastatic Progress and Treatment. Current Cell Science 2025, 01 https://doi.org/10.2174/0127726215318526241030055747
  19. Zachary J. Bernstein, Taylor R. Gierke, Kris Dammen-Brower, Stephany Y. Tzeng, Stanley Zhu, Sabrina S. Chen, D. Scott Wilson, Jordan J. Green, Kevin J. Yarema, Jamie B. Spangler. Production of site-specific antibody conjugates using metabolic glycoengineering and novel Fc glycovariants. Journal of Biological Chemistry 2024, 300 (12) , 108005. https://doi.org/10.1016/j.jbc.2024.108005
  20. Vojtěch Hamala, Kateřina Ondrášková, Lucie Červenková Šťastná, Aleš Krčil, Monika Müllerová, Martin Kurfiřt, Kateřina Hiršová, Jitka Holčáková, Róbert Gyepes, Ivana Císařová, Jana Bernášková, Roman Hrstka, Jindřich Karban. Improving the anticancer activity of fluorinated glucosamine and galactosamine analogs by attachment of a ferrocene or ruthenium tetrazene motif. Applied Organometallic Chemistry 2024, 38 (5)https://doi.org/10.1002/aoc.7399
  21. Kris Dammen‐Brower, Elaine Tan, Ruben T. Almaraz, Jian Du, Kevin J. Yarema. Protocol Considerations for In Vitro Metabolic Glycoengineering of Non‐Natural Glycans. Current Protocols 2023, 3 (6)https://doi.org/10.1002/cpz1.822
  22. Monika Chaudhary, Renu Tushir, Neetu Chopra. Polymer–drug conjugation using ester and ortho-ester bond: Mechanism, protocols, and applications. 2023, 121-145. https://doi.org/10.1016/B978-0-323-91663-9.00015-1
  23. Seth D. Ludwig, Zachary J. Bernstein, Christian Agatemor, Kris Dammen-Brower, Jeffrey Ruffolo, Jonah M. Rosas, Jeremy D. Post, Robert N. Cole, Kevin J. Yarema, Jamie B. Spangler. A versatile design platform for glycoengineering therapeutic antibodies. mAbs 2022, 14 (1)https://doi.org/10.1080/19420862.2022.2095704
  24. Fabrizio Pertusati, James Morewood. Synthesis of 2‐Acetamido‐1,3,4‐Tri‐O‐Acetyl‐2‐Deoxy‐D‐Mannopyranose ‐6‐Phosphate Prodrugs as Potential Therapeutic Agents. Current Protocols 2022, 2 (8)https://doi.org/10.1002/cpz1.500
  25. Kris Dammen-Brower, Paige Epler, Stanley Zhu, Zachary J. Bernstein, Paul R. Stabach, Demetrios T. Braddock, Jamie B. Spangler, Kevin J. Yarema. Strategies for Glycoengineering Therapeutic Proteins. Frontiers in Chemistry 2022, 10 https://doi.org/10.3389/fchem.2022.863118
  26. Vojtěch Hamala, Lucie Červenková Šťastná, Martin Kurfiřt, Petra Cuřínová, Martin Balouch, Roman Hrstka, Petr Voňka, Jindřich Karban. The effect of deoxyfluorination and O -acylation on the cytotoxicity of N -acetyl- d -gluco- and d -galactosamine hemiacetals. Organic & Biomolecular Chemistry 2021, 19 (20) , 4497-4506. https://doi.org/10.1039/D1OB00497B
  27. Nichole J. Pedowitz, Matthew R. Pratt. Design and synthesis of metabolic chemical reporters for the visualization and identification of glycoproteins. RSC Chemical Biology 2021, 2 (2) , 306-321. https://doi.org/10.1039/D1CB00010A
  28. Afraz Subratti, Antonio Ramkissoon, Lorale J. Lalgee, Nigel K. Jalsa. Synthesis and evaluation of the antibiotic-adjuvant activity of carbohydrate-based phosphoramidate derivatives. Carbohydrate Research 2021, 500 , 108216. https://doi.org/10.1016/j.carres.2020.108216
  29. Emma G. Jackson, Nichole J. Pedowitz, Matthew R. Pratt. Metabolic Engineering of Glycans. 2021, 275-287. https://doi.org/10.1016/B978-0-12-409547-2.14919-4
  30. Christian Agatemor, Keerthana Muthiah, Lisa Ha, Jacqueline Chai, Adam Osman, Bailey M. Robertson, Kevin J. Yarema. Imaging Glycans With Metabolic Glycoengineering. 2021, 253-274. https://doi.org/10.1016/B978-0-12-409547-2.14962-5
  31. Paul R. Stabach, Kristin Zimmerman, Aaron Adame, Dillon Kavanagh, Christopher T. Saeui, Christian Agatemor, Shawn Gray, Wenxiang Cao, Enrique M. De La Cruz, Kevin J. Yarema, Demetrios T. Braddock. Improving the Pharmacodynamics and In Vivo Activity of ENPP1‐Fc Through Protein and Glycosylation Engineering. Clinical and Translational Science 2021, 14 (1) , 362-372. https://doi.org/10.1111/cts.12887
  32. Joseph L. Mertz, Shisheng Sun, Bojiao Yin, Yingwei Hu, Rahul Bhattacharya, Michael J. Bettenbaugh, Kevin J. Yarema, Hui Zhang. Comparison of Three Glycoproteomic Methods for the Analysis of the Secretome of CHO Cells Treated with 1,3,4-O-Bu3ManNAc. Bioengineering 2020, 7 (4) , 144. https://doi.org/10.3390/bioengineering7040144
  33. Narek Darabedian, Bo Yang, Richie Ding, Giuliano Cutolo, Balyn W. Zaro, Christina M. Woo, Matthew R. Pratt. O-Acetylated Chemical Reporters of Glycosylation Can Display Metabolism-Dependent Background Labeling of Proteins but Are Generally Reliable Tools for the Identification of Glycoproteins. Frontiers in Chemistry 2020, 8 https://doi.org/10.3389/fchem.2020.00318
  34. Christopher T. Saeui, Kyung-cho Cho, Vrinda Dharmarha, Alison V. Nairn, Melina Galizzi, Sagar R. Shah, Prateek Gowda, Marian Park, Melissa Austin, Amelia Clarke, Edward Cai, Matthew J. Buettner, Ryan Ariss, Kelley W. Moremen, Hui Zhang, Kevin J. Yarema. Cell Line-, Protein-, and Sialoglycosite-Specific Control of Flux-Based Sialylation in Human Breast Cells: Implications for Cancer Progression. Frontiers in Chemistry 2020, 8 https://doi.org/10.3389/fchem.2020.00013
  35. Christian Agatemor, Matthew J. Buettner, Ryan Ariss, Keerthana Muthiah, Christopher T. Saeui, Kevin J. Yarema. Exploiting metabolic glycoengineering to advance healthcare. Nature Reviews Chemistry 2019, 3 (10) , 605-620. https://doi.org/10.1038/s41570-019-0126-y
  36. Qiong Wang, Cheng‐Yu Chung, Weiming Yang, Ganglong Yang, Sandra Chough, Yiqun Chen, Bojiao Yin, Rahul Bhattacharya, Yingwei Hu, Christopher T. Saeui, Kevin J. Yarema, Michael J. Betenbaugh, Hui Zhang. Combining Butyrated ManNAc with Glycoengineered CHO Cells Improves EPO Glycan Quality and Production. Biotechnology Journal 2019, 14 (4)https://doi.org/10.1002/biot.201800186
  37. Sam J Moons, Gosse J Adema, Max TGM Derks, Thomas J Boltje, Christian Büll. Sialic acid glycoengineering using N-acetylmannosamine and sialic acid analogs. Glycobiology 2019, 3 https://doi.org/10.1093/glycob/cwz026
  38. Sung-Uk Lee, Carey F. Li, Christie-Lynn Mortales, Judy Pawling, James W. Dennis, Ani Grigorian, Michael Demetriou, . Increasing cell permeability of N-acetylglucosamine via 6-acetylation enhances capacity to suppress T-helper 1 (TH1)/TH17 responses and autoimmunity. PLOS ONE 2019, 14 (3) , e0214253. https://doi.org/10.1371/journal.pone.0214253
  39. Matthew J. Buettner, Sagar R. Shah, Christopher T. Saeui, Ryan Ariss, Kevin J. Yarema. Improving Immunotherapy Through Glycodesign. Frontiers in Immunology 2018, 9 https://doi.org/10.3389/fimmu.2018.02485
  40. Bojiao Yin, Qiong Wang, Cheng‐Yu Chung, Xiaozhi Ren, Rahul Bhattacharya, Kevin J. Yarema, Michael J. Betenbaugh. Butyrated ManNAc analog improves protein expression in Chinese hamster ovary cells. Biotechnology and Bioengineering 2018, 115 (6) , 1531-1541. https://doi.org/10.1002/bit.26560
  41. Christopher T. Saeui, Alison V. Nairn, Melina Galizzi, Christopher Douville, Prateek Gowda, Marian Park, Vrinda Dharmarha, Sagar R. Shah, Amelia Clarke, Melissa Austin, Kelley W. Moremen, Kevin J. Yarema, . Integration of genetic and metabolic features related to sialic acid metabolism distinguishes human breast cell subtypes. PLOS ONE 2018, 13 (5) , e0195812. https://doi.org/10.1371/journal.pone.0195812
  42. Wilson R. Sinclair, Jonathan H. Shrimp, Thomas T. Zengeya, Rhushikesh A. Kulkarni, Julie M. Garlick, Hans Luecke, Andrew J. Worth, Ian A. Blair, Nathaniel W. Snyder, Jordan L. Meier. Bioorthogonal pro-metabolites for profiling short chain fatty acylation. Chemical Science 2018, 9 (5) , 1236-1241. https://doi.org/10.1039/C7SC00247E
  43. Jack T. Bragg, Hannah K. D'Ambrosio, Timothy J. Smith, Caroline A. Gorka, Faraz A. Khan, Joshua T. Rose, Andrew J. Rouff, Terence S. Fu, Brittany J. Bisnett, Michael Boyce, Sudhir Khetan, Margot G. Paulick. Esterified Trehalose Analogues Protect Mammalian Cells from Heat Shock. ChemBioChem 2017, 18 (18) , 1863-1870. https://doi.org/10.1002/cbic.201700302
  44. Bojiao Yin, Qiong Wang, Cheng‐Yu Chung, Rahul Bhattacharya, Xiaozhi Ren, Juechun Tang, Kevin J. Yarema, Michael J. Betenbaugh. A novel sugar analog enhances sialic acid production and biotherapeutic sialylation in CHO cells. Biotechnology and Bioengineering 2017, 114 (8) , 1899-1902. https://doi.org/10.1002/bit.26291
  45. Mohit P. Mathew, Elaine Tan, Jason W. Labonte, Shivam Shah, Christopher T. Saeui, Lingshu Liu, Rahul Bhattacharya, Patawut Bovonratwet, Jeffrey J. Gray, Kevin J. Yarema. Glycoengineering of Esterase Activity through Metabolic Flux‐Based Modulation of Sialic Acid. ChemBioChem 2017, 18 (13) , 1204-1215. https://doi.org/10.1002/cbic.201600698
  46. Haitham A. Badr, Dina M.M. AlSadek, Motawa E. El-Houseini, Christopher T. Saeui, Mohit P. Mathew, Kevin J. Yarema, Hafiz Ahmed. Harnessing cancer cell metabolism for theranostic applications using metabolic glycoengineering of sialic acid in breast cancer as a pioneering example. Biomaterials 2017, 116 , 158-173. https://doi.org/10.1016/j.biomaterials.2016.11.044
  47. Yoshihiro Ueda. Final-stage Site-selective Acylation for the Total Synthesis of Natural Glycosides. YAKUGAKU ZASSHI 2016, 136 (12) , 1631-1639. https://doi.org/10.1248/yakushi.16-00186
  48. Mohit P. Mathew, Elaine Tan, Christopher T. Saeui, Patawut Bovonratwet, Samuel Sklar, Rahul Bhattacharya, Kevin J. Yarema. Metabolic flux-driven sialylation alters internalization, recycling, and drug sensitivity of the epidermal growth factor receptor (EGFR) in SW1990 pancreatic cancer cells. Oncotarget 2016, 7 (41) , 66491-66511. https://doi.org/10.18632/oncotarget.11582
  49. Paul R. Wratil, Rüdiger Horstkorte, Werner Reutter. Metabolisches Glykoengineering mit N ‐Acyl‐Seiten‐ ketten‐modifizierten Mannosaminen. Angewandte Chemie 2016, 128 (33) , 9632-9665. https://doi.org/10.1002/ange.201601123
  50. Paul R. Wratil, Rüdiger Horstkorte, Werner Reutter. Metabolic Glycoengineering with N ‐Acyl Side Chain Modified Mannosamines. Angewandte Chemie International Edition 2016, 55 (33) , 9482-9512. https://doi.org/10.1002/anie.201601123
  51. Štěpán Horník, Lucie Červenková Šťastná, Petra Cuřínová, Jan Sýkora, Kateřina Káňová, Roman Hrstka, Ivana Císařová, Martin Dračínský, Jindřich Karban. Synthesis and in vitro cytotoxicity of acetylated 3-fluoro, 4-fluoro and 3,4-difluoro analogs of D-glucosamine and D-galactosamine. Beilstein Journal of Organic Chemistry 2016, 12 , 750-759. https://doi.org/10.3762/bjoc.12.75
  52. Yoshihiro Ueda, Takumi Furuta, Takeo Kawabata. Final‐Stage Site‐Selective Acylation for the Total Syntheses of Multifidosides A–C. Angewandte Chemie 2015, 127 (41) , 12134-12138. https://doi.org/10.1002/ange.201504729
  53. Yoshihiro Ueda, Takumi Furuta, Takeo Kawabata. Final‐Stage Site‐Selective Acylation for the Total Syntheses of Multifidosides A–C. Angewandte Chemie International Edition 2015, 54 (41) , 11966-11970. https://doi.org/10.1002/anie.201504729
  54. Mohit P. Mathew, Elaine Tan, Christopher T. Saeui, Patawut Bovonratwet, Lingshu Liu, Rahul Bhattacharya, Kevin J. Yarema. Metabolic glycoengineering sensitizes drug-resistant pancreatic cancer cells to tyrosine kinase inhibitors erlotinib and gefitinib. Bioorganic & Medicinal Chemistry Letters 2015, 25 (6) , 1223-1227. https://doi.org/10.1016/j.bmcl.2015.01.060
  55. Jeannine M. Coburn, Luccie Wo, Nicholas Bernstein, Rahul Bhattacharya, Udayanath Aich, Clifton O. Bingham, Kevin J. Yarema, Jennifer H. Elisseeff. Short-Chain Fatty Acid-Modified Hexosamine for Tissue-Engineering Osteoarthritic Cartilage. Tissue Engineering Part A 2013, 19 (17-18) , 2035-2044. https://doi.org/10.1089/ten.tea.2012.0317
  56. Jeannine M. Coburn, Nicholas Bernstein, Rahul Bhattacharya, Udayanath Aich, Kevin J. Yarema, Jennifer H. Elisseeff, . Differential Response of Chondrocytes and Chondrogenic-Induced Mesenchymal Stem Cells to C1-OH Tributanoylated N-Acetylhexosamines. PLoS ONE 2013, 8 (3) , e58899. https://doi.org/10.1371/journal.pone.0058899
  57. Nils Bayer, Uwe Schubert, Zehra Sentürk, Silvia Rudloff, Sandra Frank, Heike Hausmann, Hildegard Geyer, Rudolf Geyer, Klaus Preissner, Sebastian Galuska. Artificial and Natural Sialic Acid Precursors Influence the Angiogenic Capacity of Human Umbilical Vein Endothelial Cells. Molecules 2013, 18 (3) , 2571-2586. https://doi.org/10.3390/molecules18032571
  58. Jürgen Seibel, Simone König, Antonia Göhler, Sören Doose, Elisabeth Memmel, Nadja Bertleff, Markus Sauer. Investigating infection processes with a workflow from organic chemistry to biophysics: the combination of metabolic glycoengineering, super-resolution fluorescence imaging and proteomics. Expert Review of Proteomics 2013, 10 (1) , 25-31. https://doi.org/10.1586/epr.12.72
  59. Cindy J. Carroux, Janina Moeker, Josephine Motte, Marie Lopez, Laurent F. Bornaghi, Kasiram Katneni, Eileen Ryan, Julia Morizzi, David M. Shackleford, Susan A. Charman, Sally-Ann Poulsen. Synthesis of acylated glycoconjugates as templates to investigate in vitro biopharmaceutical properties. Bioorganic & Medicinal Chemistry Letters 2013, 23 (2) , 455-459. https://doi.org/10.1016/j.bmcl.2012.11.056
  60. Mohit P. Mathew, Elaine Tan, Shivam Shah, Rahul Bhattacharya, M. Adam Meledeo, Jun Huang, Freddy A. Espinoza, Kevin J. Yarema. Extracellular and intracellular esterase processing of SCFA–hexosamine analogs: Implications for metabolic glycoengineering and drug delivery. Bioorganic & Medicinal Chemistry Letters 2012, 22 (22) , 6929-6933. https://doi.org/10.1016/j.bmcl.2012.09.017
  61. Ruben T. Almaraz, Yuan Tian, Rahul Bhattarcharya, Elaine Tan, Shih-Hsun Chen, Matthew R. Dallas, Li Chen, Zhen Zhang, Hui Zhang, Konstantinos Konstantopoulos, Kevin J. Yarema. Metabolic Flux Increases Glycoprotein Sialylation: Implications for Cell Adhesion and Cancer Metastasis. Molecular & Cellular Proteomics 2012, 11 (7) , M112.017558-1-M112.017558-12. https://doi.org/10.1074/mcp.M112.017558
  62. Long Chen, Jun F. Liang. Metabolic monosaccharides altered cell responses to anticancer drugs. European Journal of Pharmaceutics and Biopharmaceutics 2012, 81 (2) , 339-345. https://doi.org/10.1016/j.ejpb.2012.03.012
  63. Ruben T. Almaraz, Mohit P. Mathew, Elaine Tan, Kevin J. Yarema. Metabolic Oligosaccharide Engineering: Implications for Selectin-Mediated Adhesion and Leukocyte Extravasation. Annals of Biomedical Engineering 2012, 40 (4) , 806-815. https://doi.org/10.1007/s10439-011-0450-y
  64. Ruben T. Almaraz, Udayanath Aich, Hargun S. Khanna, Elaine Tan, Rahul Bhattacharya, Shivam Shah, Kevin J. Yarema. Metabolic oligosaccharide engineering with N ‐Acyl functionalized ManNAc analogs: Cytotoxicity, metabolic flux, and glycan‐display considerations. Biotechnology and Bioengineering 2012, 109 (4) , 992-1006. https://doi.org/10.1002/bit.24363
  65. Jian Du, Pao-Lin Che, Udayanath Aich, Elaine Tan, Hyo Jun Kim, Srinivasa-Gopalan Sampathkumar, Kevin J. Yarema. Deciphering glycan linkages involved in Jurkat cell interactions with gold-coated nanofibers via sugar-displayed thiols. Bioorganic & Medicinal Chemistry Letters 2011, 21 (17) , 4980-4984. https://doi.org/10.1016/j.bmcl.2011.05.044
  66. Elaine Tan, Ruben T. Almaraz, Hargun S. Khanna, Jian Du, Kevin J. Yarema. Experimental Design Considerations for In Vitro Non‐Natural Glycan Display via Metabolic Oligosaccharide Engineering. Current Protocols in Chemical Biology 2010, 2 (3) , 171-194. https://doi.org/10.1002/9780470559277.ch100059
  67. Udayanath Aich, M. Adam Meledeo, Srinivasa-Gopalan Sampathkumar, Jie Fu, Mark B. Jones, Christopher A. Weier, Sung Yun Chung, Benjamin C. Tang, Ming Yang, Justin Hanes, Kevin J. Yarema. Development of delivery methods for carbohydrate-based drugs: controlled release of biologically-active short chain fatty acid-hexosamine analogs. Glycoconjugate Journal 2010, 27 (4) , 445-459. https://doi.org/10.1007/s10719-010-9292-3
  68. Chad M. Whitman, Michelle R. Bond, Jennifer J. Kohler. Chemical Glycobiology. 2010, 175-224. https://doi.org/10.1016/B978-008045382-8.00681-X
  69. Jian Du, M Adam Meledeo, Zhiyun Wang, Hargun S Khanna, Venkata D P Paruchuri, Kevin J Yarema. Metabolic glycoengineering: Sialic acid and beyond. Glycobiology 2009, 19 (12) , 1382-1401. https://doi.org/10.1093/glycob/cwp115
  70. Zhiyun Wang, Jian Du, Pao-Lin Che, M Adam Meledeo, Kevin J Yarema. Hexosamine analogs: from metabolic glycoengineering to drug discovery. Current Opinion in Chemical Biology 2009, 13 (5-6) , 565-572. https://doi.org/10.1016/j.cbpa.2009.08.001
  71. Prabhani U. Atukorale, Sean S. Choi, Udayanath Aich, Christopher T. Campbell, M. Adam Meledeo, Kevin J. Yarema. Chemical Biology of Cell Surface Oligosaccharides. 2009, 189-222. https://doi.org/10.1002/9780470495018.ch10
  72. Michelle R Bond, Haochi Zhang, Peter D Vu, Jennifer J Kohler. Photocrosslinking of glycoconjugates using metabolically incorporated diazirine-containing sugars. Nature Protocols 2009, 4 (7) , 1044-1063. https://doi.org/10.1038/nprot.2009.85
  73. Doug Auld, Anton Simeonov, Craig Thomas. Literature Search and Review. ASSAY and Drug Development Technologies 2008, 6 (3) , 307-326. https://doi.org/10.1089/adt.2008.9991

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