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Facile Synthesis of Mesocrystalline SnO2 Nanorods on Reduced Graphene Oxide Sheets: An Appealing Multifunctional Affinity Probe for Sequential Enrichment of Endogenous Peptides and Phosphopeptides Wen Ma,∥,† Feng Zhang,∥,‡ Liping Li,§ Shuai Chen,‡ Limin Qi,*,‡ Huwei Liu,† and Yu Bai*,† †
Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, College of Chemistry, Peking University, Beijing, 100871, PR China ‡ Beijing National Laboratory for Molecular Sciences, State Key Laboratory for Structural Chemistry of Stable and Unstable Species, College of Chemistry, Peking University, Beijing 100871, PR China § Department of Chemistry, Capital Normal University, Beijing 100048, PR China S Supporting Information *
ABSTRACT: A novel multifunctional composite comprising mesocrystalline SnO2 nanorods (NRs) vertically aligned on reduced graphene oxide (rGO) sheets was synthesized and developed for sequential capture of endogenous peptides and phosphopeptides. With the hydrophobicity of rGO and high affinity of SnO2 nanorods, sequential enrichment of endogenous peptides and phosphopeptides could be easily achieved through a modulation of elution buffer. With this multifunctional nanomaterial, 36 peptides were observed from diluted bovine serum albumin (BSA) tryptic digest and 4 phosphopeptides could be selectively captured from β-casein digest. The detection limit of tryptic digest of β-casein was low to 4 × 10−10 M, and the selectivity was up to 1:500 (molar ratio of βcasein and BSA digest). The effectiveness and robustness of rGO-SnO2 NRs in a complex biological system was also confirmed by using human serum as a real sample. Our work is promising for small peptide enrichment and identification especially in complicated biological sample preparation, which also opens a new perspective in the design of multifunctional affinity probes for proteome or peptidome. KEYWORDS: phosphopeptides, endogenous peptides, multifunctional affinity probe, sequential enrichment, mass spectrometry
1. INTRODUCTION Low-abundance endogenous peptides and phosphopeptides play crucial roles in many physiological and pathological processes.1 Changes of these two types of peptides in body fluid have a direct relation to many human pathologies;2 thus, related research is of great value for clinical diagnosis and significant biomarker discovery. However, the analysis of endogenous peptides remains a challenging task because of the severe interference from highly abundant proteins, salts, and other contaminants in a complex matrix.3 On the other hand, the low ionization efficiency and stoichiometry, together with the severe suppression by abundant nontarget peptides, greatly limit the direct analysis of phosphorylation by mass spectrometry (MS).4 Powerful sample pretreatment techniques prior to MS analysis have long been in urgent demand. Diversified approaches have been explored for purification and separation of endogenous peptides or phosphopeptides. Carbon nanomaterials, such as carbon nanotube5 and ordered mesoporous carbon material,6 have been investigated as novel © XXXX American Chemical Society
sorbents for endogenous peptides enrichment with high sensitivity. Related research confirmed that the hydrophobic interactions and π-stacking interactions are the major driving forces for the affinity between carbon nanomaterials and peptides/proteins.7 For phosphoproteome research, multiple strategies based on immobolized metal ion affinity chromatography (IMAC), 8 metal oxide affinity chromatography (MOAC),9 and amine-based methods10 have been attempted. These affinity probes showed preference toward phosphopeptides while losing other informative peptides, thus limiting the practical use. Recently, multifunctional probes targeting the enrichment of different types of peptides have aroused great attention because of the sequential analysis of two kinds of proteins and peptides.11 Comprehensive proteome analysis could be achieved by global enrichment of peptides with Received: November 14, 2016 Accepted: December 7, 2016 Published: December 7, 2016 A
DOI: 10.1021/acsami.6b14597 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
Research Article
ACS Applied Materials & Interfaces
2.2. Characterization. Fourier-transformed infrared spectroscopy (FT-IR) characterization was carried out with KBr pellet using Bruker Tensor 27 FT-IR instrument. The transmittance spectrum was acquired with a resolution of 4 cm−1, and the average spectrum of 32 time measurements was recorded. The morphology and microstructure were characterized using scanning electron microscopy (SEM, Hitachi S4800, 10 kV) and transmission electron microscopy (TEM, FEI Tecnai F30, 300 kV). X-ray photoelectron spectroscopy (XPS) spectra were obtained from an Imaging Photoelectron Spectrometer (Axis Ultra, Kratos Analytical Ltd.). X-ray diffraction (XRD) was performed on a Rigaku DMAX-2000 instrument (Cu Kα radiation). 2.3. Synthesis of Multifunctional Affinity Probe rGO-SnO2 NRs. In detail, 3 mmol of NaBr and 0.1 mmol of SnCl4·5H2O were dissolved in 1 mL of GO aqueous dispersion (0.8 mg mL−1) and 6 mL of glacial acetic acid, respectively. Then, 1 mL of ethanol was added and the mixture was stirred continuously. The mixed solution comprising three solvents was then transferred into a 25 mL Teflonlined stainless steel autoclave, and the reaction was conducted at 200 °C for 24 h to get a black power. The resultant black product was separated by centrifugation treatment, washed by deionized water and ethanol for three times each, and dried in a vacuum oven overnight to form GO-SnO2 NRs. To obtain rGO-SnO2 NRs, the produced GOSnO2 was annealed at 600 °C in argon atmosphere for 6 h with a temperature ramp of 5 °C min−1. 2.4. Enrichment of Peptides in BSA and Phosphopeptides in β-Casein. For low-abundance peptides enrichment in BSA, 200 μg of rGO-SnO2 NRs was added to 200 μL of diluted tryptic digest of BSA (1.5 × 10−7 M). The mixture was incubated for 30 min in water. After being washed by water three times, the adsorbed peptides were eluted with elution buffer containing ACN/H2O/TFA (80:19.8:0.2, v/v/v). The collected peptides were analyzed by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDITOF MS) or liquid chromatography−tandem mass spectrometry (LC-MS/MS). For phosphopeptide enrichment in β-casein, tryptic digest of β-casein was diluted into a certain concentration in loading buffer containing H2O/ACN/TFA (90:9.8:0.2, v/v/v). A 100 μg sample of the material was added to 200 μL of tryptic digest of βcasein, and the mixture was then shaken for 30 min. A solution containing H2O/ACN/TFA (50:49.8:0.2, v/v/v) was used as washing buffer to remove other nonphosphopeptides; the adsorbed phosphopeptides were eluted with 0.4 M NH4OH. The collected peptides were analyzed by MALDI-TOF MS. 2.5. Sequential Enrichment of Endogenous Peptides and Phosphopeptides in Complex Sample. A 20 μL sample of human serum was 10-fold diluted by water, followed by incubation with 400 μg of rGO-SnO2 NRs for 30 min. The enriched peptides were eluted by buffer containing ACN/H2O/TFA (80:19.8:0.2, v/v/v). Subsequently, the rGO-SnO2 NRs composite was further washed by the above-mentioned buffer twice to purify phosphopeptides. After that, the trapped phosphopeptides were eluted by 0.4 M NH4OH. The collected peptides were collected for LC-MS/MS or MALDI-TOF MS analysis. 2.6. Mass Spectrometry Analysis. MALDI-TOF MS spectra were obtained by a Bruker Daltonics ultraflex TOF mass spectrometer in reflection mode. A mixture of ACN/H2O (1:1, v/v) containing 20 mg/mL DHB and 5% H3PO4 was prepared as the matrix. For eluted peptides, 0.5 μL of elute was mixed with 0.5 μL of matrix on the steel plate for MS analysis. All LC-MS/MS measurements were performed on a Velos Pro Orbitrap Elite mass spectrometer (Thermo Scientific, United States) equipped with a nano-electrospray ionization source. The samples were vacuum-centrifuged to dryness, reconstituted in 0.2% formic acid, loaded onto a 100 μm × 1.5 cm precolumn, and separated on a 75 μm × 15 cm capillary column with laser-pulled sprayer. Both columns were packed in-house with 4 μm C18 bulk material (InnosepBio, PR China). For a gradient separation, 5−28% B in 29 min, 28%−75% B in 6 min, then held at 75% B for 18 min (A = 0.1% formic acid in water; B = 0.1% formic acid in acetonitrile). The mass spectrometer was operated in data-dependent mode with a full MS scan in FT mode (m/z 375−1600) at a resolution of 120 000
subsequent detection of phosphopeptides. Some newly developed materials were fabricated to meet the demand to extract endogenous peptides and phosphopeptides synchronously.12,13 However, complicated synthetic techniques were usually required for different nanomaterials in developing such composites. Such a tedious synthetic route and a relatively low grafting efficiency of functional moieties on the substrates greatly limits the extraction efficacy, thus leading to a poor enrichment selectivity. Therefore, a multifunctional affinity probe prepared by a facile synthesis procedure for sequential enrichment of endogenous peptides and phosphopeptides with high sensitivity and selectivity was of significant value for obtaining more comprehensive information on proteome. Graphene-based materials have attracted a great deal of interest in recent decades.14 The unique characteristics such as ultrahigh specific surface area, π-electron structure, and mechanical strength make them widely used in electrocatalysts,15 biosensors,16 gas storage,17 and electrochemical devices.18 Recently, a series of new sorbents based on graphene were developed for selective adsorption of biomolecules such as peptides,19 fatty acid,20 and amino acids21 because of their high adsorption capacity and hydrophobic interaction. SnO2, as one of the MOAC probes, has been identified as an appealing affinity probe for phosphopeptide enrichment and has shown more excellent selectivity and less nonspecific binding than TiO2.22 Various SnO2-based materials have been investigated to improve the performance in phosphoproteomic research.23−25 However, the possibility of developing a SnO2-based multifunctional affinity probe has never been explored. Herein, a binary composite consisting of mesocrystalline SnO2 nanorods on reduced graphene oxide sheets (rGO-SnO2 NRs) was innovatively designed for sequential enrichment of endogenous peptides and phosphopeptides. Compared with other peptide affinity probes, our rGO-SnO2 NRs probe has obvious merits in three aspects. First, the simple synthesis procedure consists of only a solvothermal method followed by thermal reduction. Second, the hydrophobicity of rGO and the relatively high density of SnO2 nanorods directly grown on the surface of rGO facilitates the high selectivity and sensitivity toward peptide enrichment. Third, sequential enrichment toward phosphopeptides and endogenous peptides could be easily achieved through a modulation of elution buffer, thus offering a relatively simple method for overall proteome analysis. In summary, such a multifunctional affinity probe could easily simplify the sample complexity and contribute to the practical application in the biological sample preparation. Meanwhile, it opens a new perspective in the design of a multifunctional affinity probe using novel nanomaterials in proteome research.
2. EXPERIMENTAL SECTION 2.1. Materials and Chemicals. Trypsin, β-casein, bovine serum albumin (BSA), and acetonitrile (ACN) were purchased from SigmaAldrich. 2,5-Dihydroxybenzoic acid (DHB) was purchased from J&K Scientific Ltd. Ammonium bicarbonate (NH4HCO3) was from Fluka. Phosphoric acid (H3PO4) was from Beijing Chemical Works. Trifluoroacetic acid (TFA) was obtained from Acros Organics. Graphene oxide (GO) was purchased from Nanjing XFNANO Materials Tech Co., Ltd. SnCl4·5H2O was from Sinopharm Chemical Reagent Co., Ltd. NaBr was from Xilong Chemical Co., Ltd. Water used for digestion and enrichment analysis was from Wahaha Group Co., Ltd. All chemicals were of analytical grade except ACN, which was of HPLC grade. Human serum of a healthy person was obtained from Peking University Hospital. B
DOI: 10.1021/acsami.6b14597 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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ACS Applied Materials & Interfaces
Scheme 1. (a) Synthesis Route of rGO-SnO2 NRs and (b) the Sequential Enrichment of Low-Abundance Peptides and Phosphopeptides
followed by collision induced dissociation scans. The seven most abundant ions with charge 2+ and 3+ and above an intensity threshold of 3000 were selected for MS/MS. The dynamic exclusion was set at 20 s. The raw data files were converted to mascot generic format (“.mgf”) using MSConvert before being submitted for database search. Mascot (version 2.3.02) carried out all database searches with the following parameters: Enzyme as none; Oxidation (Met) as variable modification; ±5 ppm for peptide pass tolerance; and ±0.6 Da for fragment mass tolerance.
3. RESULTS AND DISCUSSION 3.1. Synthesis and Characterization of rGO-SnO2 NRs. In our experiment, a simple solvothermal followed by thermal reduction was proposed for the synthesis of rGO-SnO2 NRs (Scheme 1a). Mesocrystalline SnO2 nanorods were solvothermally synthesized on GO sheets in a ternary solvent system to form GO-SnO2 NRs composite. After thermal reduction, a multifunctional affinity probe rGO-SnO2 NRs with hydrophobicity and high affinity toward phosphopeptides was obtained. SEM images (Figure 1a) confirmed that mesocrystalline SnO2 nanorods were uniformly grown on rGO sheet. Moreover, the high-magnification SEM image suggested that the SnO2 nanorod was 700 nm in length and 100 nm in diameter. Impressively, each SnO2 nanorod had a square cross section and rough top surface, indicating each nanorod consisted of a bundle of primary nanorods (Figure 1b). Figure 1c is the TEM image of rGO-SnO2 NRs. The highmagnification image in Figure 1d is the top end of the SnO2 nanorod which clearly demonstrated the primary subunits. Figure 1e reveals a typical SnO 2 nanorod, and the corresponding selected-area electron diffraction (SAED) image in the inset clearly exhibits the single-crystalline diffraction patterns of rutile SnO2; this illustrated that each SnO2 nanorod was a single-crystal-like SnO2 mesocrystal with a growth orientation along the [001] direction with four side surfaces enclosed by {110} planes, which was in accordance with the mesocrystalline SnO2 nanorods on Ti foil26 and carbon nanotubes.27 As shown in Figure 1f, the lattice fringes were clearly observed in the HRTEM image. The 0.32 and 0.34 nm d spacings could be ascribed to the (001) and (110) planes of SnO2, respectively. The X-ray energy dispersive spectrum (EDS) confirmed the exsistence of C, O, and Sn elements (Figure S1). As illustrated in Figure 2, the XRD image showed that all peaks could be indexed to the rutile SnO2 (JCPDS entry
Figure 1. SEM (a, b), TEM (c−e), and HRTEM (f) images of rGOSnO2 NRs. The inset in panel e is the corresponding SAED pattern.
41-1445), which is in agreement with the SAED results in the inset in Figure 1e. As shown in FT-IR (Figure S2), two peaks at 1726 and 1630 cm−1 could be attributed to the vibration of carbonyl in −COOH on the surface of GO and −CC− of graphene structure, respectively. The disappearance of the peak at 1726 cm−1 after thermal treatment indicated the reduction of hydrophilic groups such as −COOH on GO. A new peak at 675 cm−1 can be ascribed to the −Sn−O− group. The XPS image in Figure S3 clearly shows that the multifunctional rGOSnO2 NRs consisted of C, O, and Sn elements. The deconvoluted C 1s spectrum of rGO-SnO2 NRs (Figure S3b) revealed four kinds of carbon bonds: CC/C−C (284.7 eV), C−O (286.2 eV), CO (287.7 eV), and O−CO (288.8 C
DOI: 10.1021/acsami.6b14597 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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SnO2 NRs in the enrichment of low-abundance peptides. As apparently shown in Figure 3, only nine peptides were observed with low intensity without any pretreatment. However, numerous peptides were observed after treatment with affinity probe rGO-SnO2 NRs (Figure 3b). For unambiguous verification, eluted peptides were sent into LC-MS/MS, and 36 peptides with sequence coverage over 39% were found in total (Table S1). The number of peptides enriched from BSA by using our rGO-SnO2 NRs was much more than that extracted using multifunctional LaPO4−graphene oxide composites (LaGM),12 which demonstrated the excellent performance of rGO-SnO2 NRs in low-abundance peptides enrichment. As shown in Figure 3c,d, peptide enrichment efficiencies of commercial SnO2 and as-synthesized GO-SnO2 NRs were compared. As we expected, neither of them could extract peptides efficiently. The poor performance was probably attributed to the limited hydrophobicity of materials. The S/ N ratios of eight selected peptides after enrichment with SnO2, GO-SnO2, and rGO-SnO2 are listed in Table S2. When the S/ N obtained from rGO-SnO2 was compared with those from SnO2 and GO-SnO2, the S/N ratio of m/z 1478.79 was significantly enhanced, 63-fold and 31-fold, respectively, indicating the higher efficacy of our rGO-SnO2 NRs in peptide enrichment. Furthermore, to explore the reusability of rGOSnO2 NRs, the material was washed by the elution buffer two times and then treated with BSA tryptic digest. The cleanup process clearly washed all the remaining peptides from the composites. As shown in Figure S4, the intensity and types of enriched peptides remained the same as before even after the fifth reuse; this demonstrated the good reusability of our rGOSnO2 NRs.
Figure 2. XRD pattern of rGO-SnO2 NRs.
eV). The low signal for oxygen-containing groups in rGO-SnO2 NRs demonstrated the successful synthesis of rGO during the hydrothermal process. Two peaks centered at 495.7 and 487.3 eV corresponded to Sn 3d3/2 and Sn 3d5/2, respectively. The atomic ratios of O/Sn and O/C in GO-SnO2 NRs and rGOSnO2 NRs were illustrated in Figure S3d. The O/Sn ratio was almost the same in two composites, and the approximately 30% decrease in O/C ratio was attributed to further reduction of GO, as evidenced in the FT-IR results. 3.2. Enrichment of Peptides and Phosphopeptides from Model Samples. Diluted tryptic digest of BSA was employed as a model sample to examine the efficacy of rGO-
Figure 3. MALDI-TOF MS spectra of BSA digest (1.5 × 10−7 M): (a) by direct analysis, (b) after rGO-SnO2 NRs enrichment, (c) after commercial SnO2 enrichment, and (d) after GO-SnO2 NRs enrichment. D
DOI: 10.1021/acsami.6b14597 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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Figure 4. MALDI-TOF MS spectra of (a) β-casein digest (4 × 10−7 M) without any enrichment, (b) after rGO-SnO2 NRs enrichment, and (c) highly diluted β-casein digest (4 × 10−10 M) after capture by rGO-SnO2 NRs. “#” denote dephosphorylated fragments.
Figure 5. MALDI-TOF mass spectra of peptides derived from tryptic peptide mixture of β-casein and BSA (a) before enrichment (in the molar ratio of 1:100) and (b, c, d) after enrichment by rGO-SnO2 NRs in the ratio of 1:100, 1:200, 1:500, respectively. “#” denote dephosphorylated fragments.
Phosphopeptide enrichment from tryptic digest of β-casein was also performed in as-synthesized affinity probe rGO-SnO2 NRs, as illustrated in Figure 4. To optimize the enrichment conditions, different loading buffers containing various water concentration were employed (Figure S5). Under the optimized conditions, four phosphopeptides were easily observed according to the characteristic fragment ions after phosphate loss (Table S3). In addition, powerful rGO-SnO2 NRs showed brilliant enrichment efficacy even though the βcasein tryptic digest concentration was as low as 4 × 10−10 M (Figure 4c). To explore the selectivity of rGO-SnO2 NRs for
the enrichment of phosphopeptides, peptide mixtures consisting of tryptic digest of β-casein and BSA with a different molar ratio (1:100, 1:200, or 1:500) were used (Figure 5). Before enrichment, no phosphopeptides were detected because of the severe ion suppression and serious interference caused by nontargeted peptides. However, four phosphopeptides can be selectively captured, and little interference was observed after treatment of rGO-SnO2 NRs when the molar ratio of β-casein and BSA digest was 1:200. Even when the concentration of BSA digest was 500 times greater than that of β-casein, phosphopeptides could still be observed with high intensity. In E
DOI: 10.1021/acsami.6b14597 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
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ACS Applied Materials & Interfaces contrast to LaGM12 and CeO2//SiO2−C8 Janus fibers,13 this relatively high selectivity may be due to the unique synthesis technique which ensured the direct growth of SnO2 NRs on the surface of rGO, thus providing a high density of affinity sites. The direct comparisons with these two multifunctional affinity probes are also listed in Table S4. The above features are of great importance in practical applications considering the low stoichiometry of phosphoproteins and serious interference caused by abundant contaminants in complex biological matrixes. 3.3. Sequential Enrichment of Endogenous Peptides and Phosphopeptides in a Complex Sample. Endogenous serum peptides and phosphopeptides are two important classes of potential biomarkers for the elucidation of biological and pathological variations in the serum.28 The practical effect of multifunctional affinity probe rGO-SnO2 NRs for sequential enrichment of endogenous peptides and phosphopeptides was confirmed using human serum as complex biological sample. Global peptides from serum were extracted when incubated in water. For sequential elution, the rGO-SnO2 NRs was eluted by the first acid buffer to get low-abundance endogenous peptides, then the same material was subsequently eluted by a second alkaline buffer to get phosphopeptides information. Therefore, the global enrichment with subsequent simultaneous analysis covering phosphopeptides was easily achieved through a modulation of elution buffer. As illustrated in Figure 6a, no
with low intensity were captured from the complex serum sample. However, four phosphopeptides (Figure 6c) with characteristic fragment ions were observed in subsequent second alkaline elution with high intensity. Because TiO2 is not an acceptable material for the endogenous peptide enrichment, the obvious comparison results are not shown here. The entire comparison results indicated the unique and incomparable effectiveness and robustness of our multifunctional affinity probe rGO-SnO2 NRs toward peptide enrichment in a complex biological sample.
4. CONCLUSIONS In summary, a multifunctional affinity probe rGO-SnO2 NRs was synthesized using a simple and facile solvothermal synthesis method and innovatively developed for sequential enrichment of endogenous peptides and phosphopeptides both in standard sample and serum sample through a simple modulation of elution buffer. With the combined advantages of hydrophobicity of rGO and high affinity of SnO2 NRs, this binary composite material demonstrated high sensitivity and selectivity toward peptide enrichment. Such a powerful multifunctional affinity probe provided more comprehensive information toward proteome analysis and could thus longer contribute to practical application. This work opens a new perspective in the design of a multifunctional affinity probe for proteome and peptidome research and biological sample preparation.
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.6b14597. EDS image, FT-IR spectrum, and XPS spectrum of multifunctional affinity probe rGO-SnO2 NRs; reusability of rGO-SnO2 NRs; effect of different water concentration in loading buffer on phosphopeptides captured by rGO-SnO2 NRs from β-casein digest; detailed information on low-abundance peptides and phosphopeptides enriched from digests of BSA and β-casein digest, respectively, and endogenous peptides enriched from human serum sample (PDF)
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AUTHOR INFORMATION
Corresponding Authors
*E-mail:
[email protected]. *E-mail:
[email protected]. ORCID
Yu Bai: 0000-0003-1542-0297
Figure 6. MALDI-TOF MS spectra of human serum (a) without any pretreatment, (b) after enrichment of commercial TiO2 nanoparticles, and (c) after second alkaline elution in rGO-SnO2 NRs enrichment. “#” denote dephosphorylated fragments.
Author Contributions ∥
W.M. and F.Z. contributed equally.
Notes
The authors declare no competing financial interest.
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peptides could be detected before treatment because of severe interference of high-abundant proteins, salts, and other contaminants from the complex serum matrix. However, 221 endogenous peptides can be captured in the first acid elution (Table S4) after LC-MS/MS analysis. For the comparison of the phosphopeptide enrichment using TiO2 and our rGO-SnO2 NRs, commercial TiO2 nanoparticles (200−400 nm) were selected. The phosphopeptide enrichment of commercial TiO2 was conducted using optimized conditions in the literature,29 and the result is shown in Figure 6b. Only 3 phosphopeptides
ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (21322505, 21575007, 21275012, and 21473004)
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REFERENCES
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DOI: 10.1021/acsami.6b14597 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX
