Modification of sialic acids on solid-phase: accurate characterization of. protein sialylation
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1 Supporting Information for Modification of sialic acids on solid-phase: accurate characterization of protein sialylation Shuang Yang 1,3, Lei Zhang 1, Stefani Thomas 1, Yingwei Hu 1, Shuwei Li 2, John Cipollo 3, and Hui Zhang 1 1 Department of Pathology, Johns Hopkins Medicine, Baltimore, MD 2 Institute for Bioscience and Biotechnology Research, University of Maryland College Park, Rockville, MD 3 Laboratory for Bacterial Polysaccharides, Center for Biological Evaluation and Research, Food and Drug Abstract Administration, Silver Spring, MD Sialic acids play many important roles in several physiological and pathological processes, including cancers, infection and blood diseases. Sialic acids are fragile and prone to fragmentation under electrospray ionization and matrix-assisted laser desorption/ionization. It is crucial to modify sialic acids for qualitative and quantitative identification of their change in abundance in complex biological samples. Permethylation is a method of choice for sialic acid stabilization, but the harsh conditions during permethylation may lead to the decomposition of O-acetyl groups. Esterification or amidation in solution effectively protects sialic acids, yet, it is not trivial to purify glycans from their reagents. Quantitative analysis of glycans can be achieved by labeling their reducing end using fluorescent tags. Loss of sialic acids during labeling is a major concern. In this study, we demonstrated the utility of sialic acids modification for the analysis sialyl oligosaccharides and glycopeptides. Without modification, sialic acids are partially or completely lost during sample preparation, leading to the presence of false glycans or glycopeptides in the sample. The stabilized sialic acids not only result in accurate identification of sialylated glycans, but they also improve the characterization of intact glycopeptides. The modification of sialic acids on the solid support facilitates analysis of glycans and their intact glycoproteins. S-1
2 EXPERIMENTAL PROCEDURES Materials and Chemical Reagents. Sialylglycopeptide α2,6 (SGP) was ordered from Fushimi Pharmaceutical Co., Ltd. (Marugame, Kagawa, Japan). Spin columns (snap cap) and Aminolink resin were purchased from Pierce (Thermo Fisher Scientific Inc.; Rockford, IL). HPLC grade water and acetonitrile (ACN) were purchased from Fisher Scientific. Carbograph was purchased from Grace (Columbia, MD). P-Toluidine (pt), 2,5-dihydroxybenzoic acid (DHB), N,N -dimethylaniline (DMA), formic acid (A), DMSO, hydrochloric acid (HCl), Maltoheptaose (DP7), N-(3-dimethylaminopropyl)-N - ethylcarbodiimide (EDC), phosphate buffered saline (PBS, 1x), sodium cyanoborohydride (NaCNBH 3 ), sodium carbonate, sodium citrate, Tris-HCl, and trifluoroacetic acid (TFA) were from Sigma Aldrich. NaCl (5 M) was from ChemCruz Biochemicals. Peptide-N-glycosidase F (PNGase F), denaturing buffer (10x; 400 mm dithiothreitol and 5% sodium dodecyl sulfate), and reaction buffer (G7; 10x; 500 mm sodium phosphate, ph 7.5) were purchased from New England BioLabs (Ipswich, MA). Glycoprotein Immobilization. Detailed procedures have been described in our previous studies 1-3. Briefly, proteins underwent reduction and alkylation using 1x denaturing buffer at 100 C for 10 min. Aminolink resin (50 ml slurry) was used for conjugating 20 µg protein or SGP. After conditioning the resin by ph 10 buffer (500 µl; 100 mm sodium citrate and 50 mm sodium carbonate), the sample was added to the resin (500 µl in total volume) for 4 h incubation at room temperature. The reaction was continued by adding 26.5 µl of 1 M NaCNBH 3, followed by incubation for 4 h. The resin was washed with 1x PBS twice (2000x g, 30 sec) and the reaction continued in 1x PBS in the presence of 25 mm NaCNBH3 after two washes with 1x PBS. This step required 4 h for completion, followed by 30 min blocking with 1 M Tris-HCl. The samples were stored in 4 C for further treatment. Sialic Acids in Different TFA Concentrations. We designed experiments to study the effect of TFA concentration on the hydrolysis of sialic acids. Similar to DMSO-HOAc treatment, glycoproteins were subjected to the different concentrations of TFA (0, 0.1, 1, and 10%) before or after pt-edc stabilization (SI Figure S1b). The released N-glycans were tagged by 4-plex QUANTITY to demonstrate whether S-2
3 protection first is able to prevent the acid-catalyzed hydrolysis of sialic acids. In addition, we tested the effects of different temperatures (0, 23, 37, and 65 C) and time course (1, 6, 12, 24 h) on sialic acids in the presence of 0.1% TFA (same strategy as shown in SI Figure S1). Intact Glycopeptide Stabilization on the Solid Support. Bovine fetuin (100 µg) was immobilized on the Aminolink resin by two-step capture 3. Fetuin was dissolved in 90 µl 1x ph 10 and 10 µl 10x denaturing buffer (New England BioLabs). The sample was heated at 100 C for 10 min with gentle vortexing. After cooling to room temperature, fetuin was added to pre-conditioned Aminolink resin (50 µl) and incubated for 3 h (475 µl total volume, 1x ph 10), followed by adding 25 µl 1 M NaCNBH 3 (3 h incubation). The sample was washed by 500 µl 1x PBS (twice) and incubated in 1x PBS in the presence of 50 mm NaCNBH 3 for another 3 h. The aldehyde sites on resin were blocked by 1 M Tris-HCl in the presence of 50 mm NaCNBH 3 (30 min). Samples were aliquoted equally as two subsets. One set was directly digested by trypsin and the second set underwent pt-edc modification for stabilization of sialylated glycopeptides. The pt-labeled fetuin was further digested by trypsin. Both samples were purified by C18 SPE cartridge 4, and peptides were eluted in 60% ACN (0.1% TFA). Samples were dried in a Speed-Vac (Thermo; 37 C) and resuspended in 95% ACN with 1% TFA. To test whether samples can be enriched by Oasis MAX (Waters), samples were loaded to the MAX SPE cartridge after equilibration (3 ml ACN once, 3 ml of 100 mm triethylammonium acetate (TEAA) three times, washed with 3 ml HPLC water three times, and then with 3 ml of 95% ACN/1% TFA. The flow-through from the first sample loading was re-loaded to the MAX column. The sample was then washed by buffer of 95% ACN with 1% TFA (four times; 3 ml per wash). The bound intact glycopeptides were eluted with 400 µl of 50% ACN with 0.1% TFA. To test the efficiency, the flow-through during sample loading was also collected. All samples were dried in a Speed- Vac and their concentration was estimated by a BCA assay (Bio-Rad). One µg of peptides was analyzed by LC-MS. S-3
4 MALDI-MS Profiling of N-glycans. MALDI-MS was conducted on a Shimadzu MAXIMA Resonance with a mass range from 850 to 6000 Da. The MALDI matrix consisted of 100 mg/ml DHB in the presence of 0.1 mm NaCl and 25 µm DP7. The DMA was added at a ratio of 0.02 µl per µl of matrix solution 5. Glycan composition was determined by precursor library matching and verified by MS/MS if necessary. All glycans were confirmed by databases listed in GlycoWorkbench 6. Quantitative Analysis by LC-ESI-MS. The QUANTITY-tagged N-glycans were quantitatively analyzed by an Orbitrap Velos mass spectrometer (Thermo Fisher Scientific). LC and MS parameters were the same as those that we used in our previous study 7. The N-glycans were enriched through Thermo Scientific Acclaim PepMap RSLC nano trap column with nanoviper fittings (5 µm particle size) (Cat No ). Separation was conducted on Thermo Scientific Acclaim PepMap 100 c18 LC columns (Cat No ). We developed a Python-based program (GIG Tool) for outputting Xcalibur raw data and searching against glycan precursors 3,8. RESULTS AND DISCUSSION Effect of acid-catalyzed hydrolysis on intact glycopeptides. Hydrolysis on sialylated glycans theoretically affects sialylated intact glycopeptides. It has been recognized that the study of intact glycopeptides can yield details on glycosites, occupancy, and the changes in site-specific glycosylation 9,10. Partial or complete loss of sialic acids undoubtedly leads to inaccurate results. It is thus significant to stabilize sialylated intact glycopeptides prior to MS analysis. We conducted a comprehensive study on bovine fetuin with and without pt stabilization using the solidphase method. For each sample set, we tested C18 eluate (Global), MAX bound eluate (MAX), and MAX flow-through (FLTH). The non-pt labeled samples that were tested by LC-MS include NP_FLTH, NP_Global, and NP_MAX; the pt stabilization samples consisted of PT_FLTH, PT_Global, and PT_MAX. MS spectra were searched using GPQuest 11 using known Fetuin N-glycans (SI Table S2) and N-linked glycopeptides (SI Table S3). SI Table S4 lists the intact glycopeptides from bovine fetuin without and with pt stabilization of sialic acids. Our data indicates: (1) MAX can enrich intact S-4
5 glycopeptides after pt labeling, while it is not highly specific for enrichment of intact glycopeptides without pt labeling. MAX is a mix-mode sorbent for intact glycopeptide enrichment 12. For example, the majority of intact glycopeptide (IFYLPAYN[N2H2S2]CTLRPVSQSAIIMTCPDCPSTSPYDLSNPR) was identified in NP_FLTH, suggesting that MAX has low capacity on this glycopeptide. On the other hand, MAX effectively enriches and identifies the high abundance intact glycopeptides. The results also indicate that the loss of sialic acids is observed on fetuin without pt stabilization. IFYLPAYN[N2H2]CTLRPVSQSAIIMTCPDCPSTSPYDLSNPR was only detected in MAX-enriched fetuin without pt labeling, while it was not detected after pt stabilization. This result suggests that pt labeling indeed can protect sialylated glycans and thus sialylated glycopeptides. REFERENCES 1. Yang, S.; Li, Y.; Shah, P.; Zhang, H., Glycomic analysis using glycoprotein immobilization for glycan extraction. Anal. Chem. 2013, 85 (11), Yang, S.; Zhang, H., Glycomic analysis of glycans released from glycoproteins using chemical immobilization and mass spectrometry. Curr. Protoc. Chem. Biol. 2014, 6, Yang, S.; Hu, Y.; Sokoll, L.; Zhang, H., Quantitative analysis of glycans using a solid-phase chemoenzymatic method. Nat. Protoc. 2017, Accept. 4. Yang, S.; Mishra, S.; Chen, L.; Zhou, J.-y.; Chan, D. W.; Chatterjee, S.; Zhang, H., Integrated glycoprotein immobilization method for glycopeptide and glycan analysis of cardiac hypertrophy. Anal. Chem. 2015, 87 (19), Yang, S.; Zhang, H., Glycan analysis by reversible reaction to hydrazide beads and mass spectrometry. Anal. Chem. 2012, 84 (5), Ceroni, A.; Maass, K.; Geyer, H.; Geyer, R.; Dell, A.; Haslam, S. M., GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans. J. Proteome Res. 2008, 7 (4), S-5
6 7. Yang, S.; Clark, D.; liu, Y.; Chen, J.; Zhang, L.; Chan, D. W.; Zhang, H., Analysis of N-glycans using chemoenzymatic AutoTip. Electrophoresis 2017, under review. 8. Yang, S.; Höti, N.; Yang, W.; Liu, Y.; Chen, L.; Li, S.; Zhang, H., Simultaneous analyses of N- linked and O-linked glycans of ovarian cancer cells using solid-phase chemoenzymatic method. Clin. Proteomics 2017, 14 (1), Thaysen-Andersen, M.; Packer, N. H., Advances in LC MS/MS-based glycoproteomics: getting closer to system-wide site-specific mapping of the N-and O-glycoproteome. Biochim. Biophys. Acta 2014, 1844 (9), Sun, S.; Shah, P.; Eshghi, S. T.; Yang, W.; Trikannad, N.; Yang, S.; Chen, L.; Aiyetan, P.; Höti, N.; Zhang, Z., Comprehensive analysis of protein glycosylation by solid-phase extraction of N-linked glycans and glycosite-containing peptides. Nat. Biotechnol. 2015, 34 (1), Toghi Eshghi, S.; Shah, P.; Yang, W.; Li, X.; Zhang, H., GPQuest: a spectral library matching algorithm for site-specific assignment of tandem mass spectra to intact N-glycopeptides. Anal. Chem. 2015, 87 (10), Kwok, W. H.; Ho, E. N.; Lau, M. Y.; Leung, G. N.; Wong, A. S.; Wan, T. S., Doping control analysis of seven bioactive peptides in horse plasma by liquid chromatography mass spectrometry. Anal. Bioanal. Chem. 2013, 405 (8), S-6
7 Supporting Information Figure S1. Schematic workflow of sialic acid treatment for acid-catalyzed hydrolysis. (a) Released N-glycans were treated at 4 C, 23 C, 37 C, and 65 C in a solution of dimethyl sulfide (DMSO)-acetic acid (AA) before or after p-toluidine modification. Relative quantification of N- glycans was conducted by 4-plex isobaric tag (QUANTITY); (b) Glycoproteins were treated by Trifluoroacetic acid (TFA) at concentration of 0, 0.1, 1, and 10% before or after p-toluidine modification. The relative abundance was also characterized by 4-plex QUANTITY. S-7
8 Supporting Information Figure S2. Schematic illustration of the loss of sialic acid in fetuin or intact glycopeptides. (a) The scheme of N2H2S2 can form different N-glycans when it loses one or two sialic acids. Two false N-glycans, N2H2S and N2H2, could be detected after partial or complete loss of sialic acids; (b) Intact glycopeptides lost their sialic acids. Sialic acids could be partially or completely lost by acid-catalyzed hydrolysis. Five intact glycopeptides could result in an additional 10 species that are falsely generated by the hydrolysis. S-8
9 Supporting Information Figure S3. The effect of TFA concentration on the acid-catalyzed hydrolysis of sialic acids from bovine fetuin. Fetuin consists of five major complex N-glycans, including N2H2S, N2H2S2, N3H3S2, N3H3S3, and N3H3S4. These fragile sialic acids can be lost during sample preparation such as incubation in low ph buffer. An increased concentration of TFA, 0, 0.1%, 1%, and 1% has been used to study the loss of sialic acids at room temperature (20-25 C). Both biantennary and triantennary glycans have increased amounts of asialo glycans (N2H2 and N3H3) without pt modification; while negligible amount was observed after pt modification. S-9
10 Supporting Information Table S1. Estimation of ph for acids used for chromatographic cleanup and LC-MS. HOAc = acetic acid; TFA = Trifluoroacetic acid. List HOAc TFA Formic acid Boric acid Citric acid Carbonic acid Phosphoric acid Density (g/ml) Molar mass (g/mol) pka Solution 30% 0.10% 0.20% 0.10% 0.10% 0.10% 0.10% Concentration (M) ph S-10
11 Supporting Information Table S2. List of composition for bovine fetuin N-glycans. N = HexNAc, H = Hexose, F = Fucose, S = Neu5Ac, and G = Neu5Gc N H F S G S-11
12 Supporting Information Table S3. The list of N-linked glycopeptides from bovine fetuin. List Glycosite-containing peptide sequence Motif 1 MNVLLLLVLCTLAMGCGATSPPQPAARPSSLLSLDCNSSYVLDIANDILQDINR NSS 2 MNVLLLLVLCTLAMGCGATSPPQPAARPSSLLSLDCNSSYVLDIANDILQDINRDR NSS 3 RIFYLPAYNCTLRPVSQSAIIMTCPDCPSTSPYDLSNPR NCT 4 IFYLPAYNCTLRPVSQSAIIMTCPDCPSTSPYDLSNPR NCT 5 IFYLPAYNCTLRPVSQSAIIMTCPDCPSTSPYDLSNPRFMETATESLAK NCT 6 GENATVNQRPANPSK NAT 7 GENATVNQRPANPSKTEELQQQNTAPTNSPTK NAT 8 IISVTCSFFNSQAPTPRGENATVNQRPANPSK NAT S-12
13 Supporting Information Table S4. Identification of intact glycopeptides after being digested from the solid support. One set of fetuin was immobilized on the solid support and digested by trypsin without sialic acid modification; the second set was digested by trypsin after sialic acid stabilization. Both fetuin samples were enriched by MAX solid-phase-extraction (SPE) column after C18 cartridge cleanup. NP-FLTH: no p- Toluidine modification-flow-through after MAX enrichment; NP-Global: no-p-toluidine modification-global peptides without MAX enrichment; NP-MAX: no-p-toluidine-modification-intact glycopeptide eluted from MAX enrichment; pt-flth: p-toluidine-modification, flow-through; pt-global: p-toluidine-modification, global peptides; pt-max: p-toluidine-modification, intact glycopeptides eluted from MAX enrichment; ND: not detected. Glycopeptide N-glycan Composition Intensity NP_FLTH NP_Global NP_MAX PT_FLTH PT_Global PT_MAX GENATVNQRPANPSK N3H3S ND GENATVNQRPANPSK N3H3S ND ND ND ND IFYLPAYNCTLRPVSQSAIIMTC PDCPSTSPYDLSNPR N2H2S ND S-13
14 IFYLPAYNCTLRPVSQSAIIMTC PDCPSTSPYDLSNPR N3H3S3 ND ND ND ND ND IFYLPAYNCTLRPVSQSAIIMTC PDCPSTSPYDLSNPR N2H2 ND ND ND ND ND MNVLLLLVLCTLAMGCGATSP PQPAARPSSLLSLDCNSSYVLD IANDILQDINRDR N1H1S1 ND ND ND ND IFYLPAYNCTLRPVSQSAIIMTC PDCPSTSPYDLSNPR N2H2S1 ND ND ND ND MNVLLLLVLCTLAMGCGATSP PQPAARPSSLLSLDCNSSYVLD IANDILQDINRDR N3H3S1 ND ND ND ND ND IFYLPAYNCTLRPVSQSAIIMTC PDCPSTSPYDLSNPR N3H3S3 ND ND ND ND ND (1) Yang, S.; Li, Y.; Shah, P.; Zhang, H. Anal. Chem. 2013, 85, (2) Yang, S.; Zhang, H. Curr. Protoc. Chem. Biol. 2014, 6, (3) Yang, S.; Hu, Y.; Sokoll, L.; Zhang, H. Nat. Protoc. 2017, Accept. (4) Yang, S.; Mishra, S.; Chen, L.; Zhou, J.-y.; Chan, D. W.; Chatterjee, S.; Zhang, H. Anal. Chem. 2015, 87, S-14
15 (5) Yang, S.; Zhang, H. Anal. Chem. 2012, 84, (6) Ceroni, A.; Maass, K.; Geyer, H.; Geyer, R.; Dell, A.; Haslam, S. M. J. Proteome Res. 2008, 7, (7) Yang, S.; Clark, D.; liu, Y.; Chen, J.; Zhang, L.; Chan, D. W.; Zhang, H. Electrophoresis 2017, under review. (8) Yang, S.; Höti, N.; Yang, W.; Liu, Y.; Chen, L.; Li, S.; Zhang, H. Clin. Proteomics 2017, 14, 3. (9) Thaysen-Andersen, M.; Packer, N. H. Biochim. Biophys. Acta 2014, 1844, (10) Sun, S.; Shah, P.; Eshghi, S. T.; Yang, W.; Trikannad, N.; Yang, S.; Chen, L.; Aiyetan, P.; Höti, N.; Zhang, Z. Nat. Biotechnol. 2015, 34, (11) Toghi Eshghi, S.; Shah, P.; Yang, W.; Li, X.; Zhang, H. Anal. Chem. 2015, 87, (12) Kwok, W. H.; Ho, E. N.; Lau, M. Y.; Leung, G. N.; Wong, A. S.; Wan, T. S. Anal. Bioanal. Chem. 2013, 405, S-15
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