A highly efficient protein corona-based proteomic analysis strategy for the discovery of pharmacodynamic biomarkers

Yuqing Meng; Jiayun Chen; Yanqing Liu; Yongping Zhu; Yin-Kwan Wong; Haining Lyu; Qiaoli Shi; Fei Xia; Liwei Gu; Xinwei Zhang; Peng Gao; Huan Tang; Qiuyan Guo; Chong Qiu; Chengchao Xu; Xiao He; Junzhe Zhang; Jigang Wang

doi:10.1016/j.jpha.2022.07.002

Volume 12 Issue 6

Dec. 2022

Turn off MathJax

Article Contents

Article Navigation > Journal of Pharmaceutical Analysis > 2022 > 12(6): 879-888

Yuqing Meng, Jiayun Chen, Yanqing Liu, Yongping Zhu, Yin-Kwan Wong, Haining Lyu, Qiaoli Shi, Fei Xia, Liwei Gu, Xinwei Zhang, Peng Gao, Huan Tang, Qiuyan Guo, Chong Qiu, Chengchao Xu, Xiao He, Junzhe Zhang, Jigang Wang. A highly efficient protein corona-based proteomic analysis strategy for the discovery of pharmacodynamic biomarkers[J]. Journal of Pharmaceutical Analysis, 2022, 12(6): 879-888. doi: 10.1016/j.jpha.2022.07.002

Citation:

Yuqing Meng, Jiayun Chen, Yanqing Liu, Yongping Zhu, Yin-Kwan Wong, Haining Lyu, Qiaoli Shi, Fei Xia, Liwei Gu, Xinwei Zhang, Peng Gao, Huan Tang, Qiuyan Guo, Chong Qiu, Chengchao Xu, Xiao He, Junzhe Zhang, Jigang Wang. A highly efficient protein corona-based proteomic analysis strategy for the discovery of pharmacodynamic biomarkers[J]. Journal of Pharmaceutical Analysis, 2022, 12(6): 879-888. doi: 10.1016/j.jpha.2022.07.002

Citation:

Yuqing Meng, Jiayun Chen, Yanqing Liu, Yongping Zhu, Yin-Kwan Wong, Haining Lyu, Qiaoli Shi, Fei Xia, Liwei Gu, Xinwei Zhang, Peng Gao, Huan Tang, Qiuyan Guo, Chong Qiu, Chengchao Xu, Xiao He, Junzhe Zhang, Jigang Wang. A highly efficient protein corona-based proteomic analysis strategy for the discovery of pharmacodynamic biomarkers[J]. Journal of Pharmaceutical Analysis, 2022, 12(6): 879-888. doi: 10.1016/j.jpha.2022.07.002

PDF( 2371 KB)

A highly efficient protein corona-based proteomic analysis strategy for the discovery of pharmacodynamic biomarkers

doi: 10.1016/j.jpha.2022.07.002

a. Artemisinin Research Center and Institute of Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing, 100700, China;
b. Department of Biological Sciences, National University of Singapore, 117543, Singapore;
c. Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China

Funds:

We gratefully acknowledge financial support from the National Key Research and Development Program of China (Grant Nos.: 2020YFA0908000 and 2020YFE0205100), the Innovation Team and Talents Cultivation Program of National Administration of Traditional Chinese Medicine (Grant No.: ZYYCXTD-C-202002), the National Natural Science Foundation of China (Grant Nos.: 82074098, 82173914, and 82141001), the CACMS Innovation Fund (Grant Nos.: CI2021A05101 and CI2021A05104), the Fundamental Research Funds for the Central Public Welfare Research Institutes (Grant Nos.: ZZ15-YQ-065, ZZ14-YQ-058, ZZ14-YQ-050, ZZ14-YQ-051, ZZ14-YQ-052, ZZ14-ND-010, ZZ15-ND-10, and ZZ14-FL-002), and the Chinese Academy of Sciences (Grant No.: YJKYYQ20210025).

Received Date: Feb. 20, 2022
Accepted Date: Jul. 12, 2022
Rev Recd Date: Jun. 19, 2022
Publish Date: Dec. 26, 2022

Abstract

Abstract

The composition of serum is extremely complex, which complicates the discovery of new pharmacodynamic biomarkers via serum proteome for disease prediction and diagnosis. Recently, nanoparticles have been reported to efficiently reduce the proportion of high-abundance proteins and enrich low-abundance proteins in serum. Here, we synthesized a silica-coated iron oxide nanoparticle and developed a highly efficient and reproducible protein corona (PC)-based proteomic analysis strategy to improve the range of serum proteomic analysis. We identified 1,070 proteins with a median coefficient of variation of 12.56% using PC-based proteomic analysis, which was twice the number of proteins identified by direct digestion. There were also more biological processes enriched with these proteins. We applied this strategy to identify more pharmacodynamic biomarkers on collagen-induced arthritis (CIA) rat model treated with methotrexate (MTX). The bioinformatic results indicated that 485 differentially expressed proteins (DEPs) were found in CIA rats, of which 323 DEPs recovered to near normal levels after treatment with MTX. This strategy can not only help enhance our understanding of the mechanisms of disease and drug action through serum proteomics studies, but also provide more pharmacodynamic biomarkers for disease prediction, diagnosis, and treatment.
- Protein corona,
- Nanoparticles,
- Mass spectrometry,
- Proteomic analysis,
- Pharmacodynamic biomarkers

FullText(HTML)

References(48)

References

J.R. Lamb, L.L. Jennings, V. Gudmundsdottir, et al., It’s in our blood: A glimpse of personalized medicine, Trends Mol. Med. 27 (2021) 20-30

N.L. Anderson, The clinical plasma proteome: A survey of clinical assays for proteins in plasma and serum, Clin. Chem. 56 (2010) 177-185

H. Zhang, E.C. Yi, X.J. Li, et al., High throughput quantitative analysis of serum proteins using glycopeptide capture and liquid chromatography mass spectrometry, Mol. Cell. Proteomics 4 (2005) 144-155

R.S. Tirumalai, K.C. Chan, D.A. Prieto, et al., Characterization of the low molecular weight human serum proteome, Mol. Cell. Proteomics 2 (2003) 1096-1103

M.S. Kim, S.M. Pinto, D. Getnet, et al., A draft map of the human proteome, Nature 509 (2014) 575-581

L. Dalle Carbonare, M. Manfredi, G. Caviglia, et al., Can half-marathon affect overall health? The yin-yang of sport, J. Proteomics 170 (2018) 80-87

L. Urbas, P. Brne, B. Gabor, et al., Depletion of high-abundance proteins from human plasma using a combination of an affinity and pseudo-affinity column, J. Chromatogr. A 1216 (2009) 2689-2694

H. Wang, K.K. Dey, P.C. Chen, et al., Integrated analysis of ultra-deep proteomes in cortex, cerebrospinal fluid and serum reveals a mitochondrial signature in Alzheimer’s disease, Mol. Neurodegener. 15 (2020), 43

K. Suhre, M.I. McCarthy, J.M. Schwenk, Genetics meets proteomics: Perspectives for large population-based studies, Nat. Rev. Genet. 22 (2021) 19-37

G.L. Hortin, D. Sviridov, N.L. Anderson, High-abundance polypeptides of the human plasma proteome comprising the top 4 logs of polypeptide abundance, Clin. Chem. 54 (2008) 1608-1616

V. Kulasingam, E.P. Diamandis, Strategies for discovering novel cancer biomarkers through utilization of emerging technologies, Nat. Clin. Pract. Oncol. 5 (2008) 588-599

P.Y. Lee, J. Osman, T.Y. Low, et al., Plasma/serum proteomics: Depletion strategies for reducing high-abundance proteins for biomarker discovery, Bioanalysis 11(2019) 1799-1812

V. Kumar, S. Ray, S. Ghantasala, et al., An integrated quantitative proteomics workflow for cancer biomarker discovery and validation in plasma, Front. Oncol. 10 (2020), 543997

Y. Li, H. Yuan, Z. Dai, et al., Integrated proteomic sample preparation with combination of on-line high-abundance protein depletion, denaturation, reduction, desalting and digestion to achieve high throughput plasma proteome quantification, Anal. Chim. Acta 1154 (2021), 338343

S.R. Saptarshi, A. Duschl, A.L. Lopata, Interaction of nanoparticles with proteins: relation to bio-reactivity of the nanoparticle, J. Nanobiotechnology 11 (2013), 26

S. Wan, P.M. Kelly, E. Mahon, et al., The “sweet” side of the protein corona: Effects of glycosylation on nanoparticle-cell interactions, ACS Nano 9 (2015) 2157-2166

M.P. Monopoli, C. Åberg, A. Salvati, et al., Biomolecular coronas provide the biological identity of nanosized materials, Nat. Nanotechnol. 7 (2012) 779-786

R.L. Pinals, D. Yang, D.J. Rosenberg, et al., Quantitative protein Corona composition and dynamics on carbon nanotubes in biological environments, Angew. Chem. Int. Ed. Engl. 59 (2020) 23668-23677

C.K. Elechalawar, M.N. Hossen, L. McNally, et al., Analysing the nanoparticle-protein corona for potential molecular target identification, J. Control. Release 322 (2020) 122-136

L. Vroman, Effect of absorbed proteins on the wettability of hydrophilic and hydrophobic solids, Nature 196 (1962) 476-477

K. Giri, K. Shameer, M.T. Zimmermann, et al., Understanding protein-nanoparticle interaction: A new gateway to disease therapeutics, Bioconjug. Chem. 25 (2014) 1078-1090

Y. Liu, J. Wang, Q. Xiong, et al., Nano-bio interactions in cancer: From therapeutics delivery to early detection, Acc. Chem. Res. 54 (2021) 291-301

M. Hadjidemetriou, S. McAdam, G. Garner, et al., The human in vivo biomolecule Corona onto PEGylated liposomes: A proof-of-concept clinical study, Adv. Mater. 31 (2019), e1803335

J.E. Blume, W.C. Manning, G. Troiano, et al., Rapid, deep and precise profiling of the plasma proteome with multi-nanoparticle protein corona, Nat. Commun. 11 (2020), 3662

V.F. Cardoso, A. Francesko, C. Ribeiro, et al., Advances in Magnetic Nanoparticles for Biomedical Applications, Adv. Healthc. Mater. 7 (2018), 1700845

Y. Zhu, P. Jiang, B. Luo, et al., Dynamic protein corona influences immune-modulating osteogenesis in magnetic nanoparticle (MNP)-infiltrated bone regeneration scaffolds: In vivo, Nanoscale 11 (2019) 6817-6827

Y. Portilla, S. Mellid, A. Paradela, et al., Iron oxide nanoparticle coatings dictate cell outcomes despite the influence of protein coronas, ACS Appl. Mater. Interfaces 13 (2021) 7924-7944

U. Sakulkhu, M. Mahmoudi, L. Maurizi, et al., Protein corona composition of superparamagnetic iron oxide nanoparticles with various physico-chemical properties and coatings, Sci. Rep. 4 (2014), 5020

D. Bonvin, D. Chiappe, M. Moniatte, et al., Methods of protein corona isolation for magnetic nanoparticles, Analyst 142 (2017) 3805-3815

L. Wang, J. Bao, L. Wang, et al., One-pot synthesis and bioapplication of amine-functionalized magnetite nanoparticles and hollow nanospheres, Chemistry 12 (2006) 6341-6347

Z.-Z. Yin, Y. Li, L.-P. Jiang, et al., Synthesis and electrocatalytic activity of haemin-functionalised iron(II, III) oxide nanoparticles, Anal. Chim. Acta 781 (2013) 48-53

T. Ozkaya, M.S. Toprak, A. Baykal, et al., Synthesis of Fe₃O₄ nanoparticles at 100 ℃ and its magnetic characterization, J. Alloys Compd. 472 (2009) 18-23

M. Ibrahim, A. Nada, D.E. Kamal, Density functional theory and FTIR spectroscopic study of carboxyl group, Indian. J. Pure. Ap. Phy. 43 (2005) 911-917

H. Rajabi-Moghaddam, M.R. Naimi-Jamal, M. Tajbakhsh, Fabrication of copper(II)-coated magnetic core-shell nanoparticles Fe₃O₄@SiO₂-2-aminobenzohydrazide and investigation of its catalytic application in the synthesis of 1,2,3-triazole compounds, Sci. Rep. 11 (2021), 2073

D.W. Kim, T.H. Kim, S. Choi, et al., Preparation of silica coated iron oxide nanoparticles using non-transferred arc plasma, Adv. Powder Technol. 23 (2012) 701-707

A. Miri, H. Najafzadeh, M. Darroudi, et al., Iron oxide nanoparticles: Biosynthesis, magnetic behavior, cytotoxic effect, ChemistryOpen 10 (2021) 327-333

N. Kamaly, O.C. Farokhzad, C. Corbo, Nanoparticle protein corona evolution: From biological impact to biomarker discovery, Nanoscale 14 (2022) 1606-1620

W. Richtering, I. Alberg, R. Zentel, Nanoparticles in the biological context: Surface morphology and protein corona formation, Small 16 (2020), 2002162

Z. Li, Y. Wang, J. Zhu, et al., Emerging well-tailored nanoparticulate delivery system based on in situ regulation of the protein corona, J. Control Release 320 (2020) 1-18

C. Corbo, R. Molinaro, A. Parodi, et al., The impact of nanoparticle protein corona on cytotoxicity, immunotoxicity and target drug delivery, Nanomedicine (Lond) 11 (2016) 81-100

H. Keshishian, M.W. Burgess, H. Specht, et al., Quantitative, multiplexed workflow for deep analysis of human blood plasma and biomarker discovery by mass spectrometry, Nat. Protoc. 12 (2017) 1683-1701

H. Keshishian, M.W. Burgess, M.A. Gillette, et al., Multiplexed, quantitative workflow for sensitive biomarker discovery in plasma yields novel candidates for early myocardial injury, Mol. Cell. Proteomics 14 (2015) 2375-2393

C.A. Sobsey, S. Ibrahim, V.R. Richard, et al., Targeted and untargeted proteomics approaches in biomarker development, Proteomics 20 (2020), e1900029

T.N. Tiambeng, D.S. Roberts, K.A. Brown, et al., Nanoproteomics enables proteoform-resolved analysis of low-abundance proteins in human serum, Nat. Commun. 11 (2020), 3903

In-depth plasma proteomics profiling with nanoparticle-based Proteograph workflow: A performance evaluation of label free and TMT multiplexing approaches. https://seer.bio/wp-content/uploads/2021/11/ASMS_2021_Campos.pdf. (Accessed 28 April 2022).

T. Cedervall, I. Lynch, S. Lindman, et al., Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles, Proc. Natl. Acad. Sci. U S A 104 (2007) 2050-2055

Y.H. Kim, J.S. Kang, Micro-computed tomography evaluation and pathological analyses of female rats with collagen-induced arthritis, J. Vet. Sci. 16 (2015) 165-171

W. Hui, D. Yu, Z. Cao, et al., Butyrate inhibit collagen-induced arthritis via Treg/IL-10/Th17 axis, Int. Immunopharmacol. 68 (2019) 226-233

Relative Articles

Supplements(0)

Cited By

Proportional views