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Protein and peptide phosphorylation regulate numerous pathological processes, however, their characterization is challenging due to their low abundance and transient nature. Therefore, nanomaterials are being developed to address this demanding task. In particular, carbon nanostructures are attracting interest as scaffolds for functional nanocomposites, yet only isolated studies exist on the topic, and little is known on the effect of nanocarbon morphology on templating nanocomposites. In this work, we compared oxidized carbon nanotubes, graphene oxide, oxidized carbon nanohorns and oxidized graphitized carbon black, as scaffolds for magnetized nanocomposites. The nanomaterials were extensively characterized with experimental and in silico techniques. Next, they were applied to phosphopeptide enrichment from cancer cell lysates for NanoHPLC-MS/MS, with selectivity as high as nearly 90% and several-thousand identification hits. Overall, new insights emerged for the understanding and the design of nanocomposites for phosphoproteomics.


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Carbon nanostructure morphology templates nanocomposites for phosphoproteomics

Show Author's information Susy Piovesana1Daniel Iglesias2Manuel Melle-Franco3Slavo Kralj4Chiara Cavaliere1Michele Melchionna2Aldo Laganà1,5Anna L. Capriotti1( )Silvia Marchesan2( )
Piazzale A. Moro 5, Dipartimento di Chimica, Sapienza Universitàdi Roma, Rome 00185, Italy
Via L. Giorgieri 1, Dipartimento di Scienze Chimiche e Farmaceutiche, Università di Trieste, Trieste 34127, Italy
CICECO, University of Aveiro, Aveiro 3810-193, Portugal
Jamova 39, Department for Materials Synthesis, Jožef Stefan Institute, Ljubljana 1000, Slovenia
Via Monteroni Campus Ecotekne, CNR NANOTEC, University of Salento, Lecce 73100, Italy

Abstract

Protein and peptide phosphorylation regulate numerous pathological processes, however, their characterization is challenging due to their low abundance and transient nature. Therefore, nanomaterials are being developed to address this demanding task. In particular, carbon nanostructures are attracting interest as scaffolds for functional nanocomposites, yet only isolated studies exist on the topic, and little is known on the effect of nanocarbon morphology on templating nanocomposites. In this work, we compared oxidized carbon nanotubes, graphene oxide, oxidized carbon nanohorns and oxidized graphitized carbon black, as scaffolds for magnetized nanocomposites. The nanomaterials were extensively characterized with experimental and in silico techniques. Next, they were applied to phosphopeptide enrichment from cancer cell lysates for NanoHPLC-MS/MS, with selectivity as high as nearly 90% and several-thousand identification hits. Overall, new insights emerged for the understanding and the design of nanocomposites for phosphoproteomics.

Keywords: nanocomposites, carbon nanotubes, graphene oxide, magnetic, carbon nanohorns, proteomics

References(45)

[1]
Malik, S.; Krasheninnikov, A. V.; Marchesan, S. Advances in nanocarbon composite materials. Beilstein J. Nanotechnol. 2018, 9, 20-21.
[2]
Eder, D. Carbon nanotube-inorganic hybrids. Chem. Rev. 2010, 110, 1348-1385.
[3]
Pérez, E. M.; Martín, N. π-π interactions in carbon nanostructures. Chem. Soc. Rev. 2015, 44, 6425-6433.
[4]
Lonkar, S. P.; Deshmukh, Y. S.; Abdala, A. A. Recent advances in chemical modifications of graphene. Nano Res. 2015, 8, 1039-1074.
[5]
Karousis, N.; Suarez-Martinez, I.; Ewels, C. P.; Tagmatarchis, N. Structure, properties, functionalization, and applications of carbon nanohorns. Chem. Rev. 2016, 116, 4850-4883.
[6]
Hirsch, A. Functionalization of single-walled carbon nanotubes. Angew. Chem., Int. Ed. 2002, 41, 1853-1859.
[7]
Kemnade, N.; Gebhardt, P.; Haselmann, G. M.; Cherevan, A.; Wilde, G.; Eder, D. How to evaluate and manipulate charge transfer and photocatalytic response at hybrid nanocarbon-metal oxide interfaces. Adv. Funct. Mater. 2018, 28, 1704730.
[8]
Eder, D.; Windle, A. H. Carbon-inorganic hybrid materials: The carbon-nanotube/TiO2 interface. Adv. Mater. 2008, 20, 1787-1793.
[9]
Melchionna, M.; Prato, M.; Fornasiero, P. Mix and match metal oxides and nanocarbons for new photocatalytic frontiers. Catal. Today 2016, 277, 202-213.
[10]
Saha, A.; Moya, A.; Kahnt, A.; Iglesias, D.; Marchesan, S.; Wannemacher, R.; Prato, M.; Vilatela, J. J.; Guldi, D. M. Interfacial charge transfer in functionalized multi-walled carbon nanotube@TiO2 nanofibres. Nanoscale 2017, 9, 7911-7921.
[11]
Beltram, A.; Melchionna, M.; Montini, T.; Nasi, L.; Fornasiero, P.; Prato, M. Making H2 from light and biomass-derived alcohols: The outstanding activity of newly designed hierarchical MWCNT/Pd@TiO2 hybrid catalysts. Green Chem. 2017, 19, 2379-2389.
[12]
Wijeratne, A. B.; Wijesundera, D. N.; Paulose, M.; Ahiabu, I. B.; Chu, W. K.; Varghese, O. K.; Greis, K. D. Phosphopeptide separation using radially aligned titania nanotubes on titanium wire. ACS Appl. Mater. Interfaces 2015, 7, 11155-11164.
[13]
Cutillas, P. R. Role of phosphoproteomics in the development of personalized cancer therapies. Proteomics Clin. Appl. 2015, 9, 383-395.
[14]
Rainer, M.; Bonn, G. K. Enrichment of phosphorylated peptides and proteins by selective precipitation methods. Bioanalysis 2015, 7, 243-252.
[15]
Von Stechow, L.; Francavilla, C.; Olsen, J. V. Recent findings and technological advances in phosphoproteomics for cells and tissues. Expert Rev. Proteomics. 2015, 12, 469-487.
[16]
Engholm-Keller, K.; Larsen, M. R. Technologies and challenges in large-scale phosphoproteomics. Proteomics 2013, 13, 910-931.
[17]
Beltran, L.; Cutillas, P. R. Advances in phosphopeptide enrichment techniques for phosphoproteomics. Amino Acids 2012, 43, 1009-1024.
[18]
Dunn, J. D.; Reid, G. E.; Bruening, M. L. Techniques for phosphopeptide enrichment prior to analysis by mass spectrometry. Mass Spectrom. Rev. 2010, 29, 29-54.
[19]
Wang, Z. G.; Lv, N.; Bi, W. Z.; Zhang, J. L.; Ni, J. Z. Development of the affinity materials for phosphorylated proteins/peptides enrichment in phosphoproteomics analysis. ACS Appl. Mater. Interfaces 2015, 7, 8377-8392.
[20]
Roberts, D. S.; Chen, B. F.; Tiambeng, T. N.; Wu Z. J.; Ge, Y.; Jin, S. Reproducible large-scale synthesis of surface silanized nanoparticles as an enabling nanoproteomics platform: Enrichment of the human heart phosphoproteome. Nano Res. 2019, 12, 1473-1481.
[21]
Deng, Z. A.; Zhao, Z.; Ning, B.; Basilio, J.; Mann, K.; Fu, J.; Gu, Y. J.; Ye, Y. Q.; Wu, X. F.; Fan, J. et al. Nanotrap-enabled quantification of KRAS-induced peptide hydroxylation in blood for cancer early detection. Nano Res. 2019, 12, 1445-1452.
[22]
Sun, N. R.; Wu, H.; Shen, X. Z.; Deng, C. H. Nanomaterials in proteomics. Adv. Funct. Mater. 2019, 29, 1900253.
[23]
Araújo, J. E.; Lodeiro, C.; Capelo, J. L.; Rodríguez-González, B.; Dos Santos, A. A.; Santos, H. M.; Fernández-Lodeiro, J. Novel nanocomposites based on a strawberry-like gold-coated magnetite (Fe@Au) for protein separation in multiple myeloma serum samples. Nano Res. 2015, 8, 1189-1198.
[24]
Fang, G. Z.; Gao, W.; Deng, Q. L.; Qian, K.; Han, H. T.; Wang, S. Highly selective capture of phosphopeptides using a nano titanium dioxide-multiwalled carbon nanotube nanocomposite. Anal. Biochem. 2012, 423, 210-217.
[25]
Lu, J.; Deng, C. L.; Zhang, X. M.; Yang, P. Y. Synthesis of Fe3O4/graphene/TiO2 composites for the highly selective enrichment of phosphopeptides from biological samples. ACS Appl. Mater. Interfaces 2013, 5, 7330-7334.
[26]
Wang, M. Y.; Deng, C. H.; Li, Y.; Zhang, X. M. Magnetic binary metal oxides affinity probe for highly selective enrichment of phosphopeptides. ACS Appl. Mater. Interfaces 2014, 6, 11775-11782.
[27]
Scida, K.; Stege, P. W.; Haby, G.; Messina, G. A.; García, C. D. Recent applications of carbon-based nanomaterials in analytical chemistry: Critical review. Anal. Chim. Acta 2011, 691, 6-17.
[28]
Melchionna, M.; Beltram, A.; Montini, T.; Monai, M.; Nasi, L.; Fornasiero, P.; Prato, M. Highly efficient hydrogen production through ethanol photoreforming by a carbon nanocone/Pd@TiO2 hybrid catalyst. Chem. Commun. 2016, 52, 764-767.
[29]
Iglesias, D.; Melle-Franco, M.; Kurbasic, M.; Melchionna, M.; Abrami, M.; Grassi, M.; Prato, M.; Marchesan, S. Oxidized nanocarbons-tripeptide supramolecular hydrogels: Shape matters!. ACS Nano 2018, 12, 5530-5538.
[30]
Iijima, S.; Yudasaka, M.; Yamada, R.; Bandow, S.; Suenaga, K.; Kokai, F.; Takahashi, K. Nano-aggregates of single-walled graphitic carbon nano-horns. Chem. Phys. Lett. 1999, 309, 165-170.
[31]
Iglesias, D.; Giuliani, A.; Melchionna, M.; Marchesan, S.; Criado, A.; Nasi, L.; Bevilacqua, M.; Tavagnacco, C.; Vizza, F.; Prato, M. et al. N-doped graphitized carbon nanohorns as a forefront electrocatalyst in highly selective O2 reduction to H2O2. Chem 2018, 4, 106-123.
[32]
Capriotti, A. L.; Cavaliere, C.; Foglia, P.; Samperi, R.; Stampachiacchiere, S.; Ventura, S.; Laganà, A. Ultra-high-performance liquid chromatography-tandem mass spectrometry for the analysis of free and conjugated natural estrogens in cow milk without deconjugation. Anal. Bioanal. Chem. 2015, 407, 1705-1719.
[33]
Cavaliere, C.; Capriotti, A. L.; Ferraris, F.; Foglia, P.; Samperi, R.; Ventura, S.; Laganà, A. Multiresidue analysis of endocrine-disrupting compounds and perfluorinated sulfates and carboxylic acids in sediments by ultra-high-performance liquid chromatography-tandem mass spectrometry. J. Chromatogr. A 2016, 1438, 133-142.
[34]
Di Corcia, A.; Marchese, S.; Samperi, R. Evaluation of graphitized carbon black as a selective adsorbent for extracting acidic organic compounds from water. J. Chromatogr. A 1993, 642, 163-174.
[35]
Piovesana, S.; Capriotti, A. L.; Cavaliere, C.; Ferraris, F.; Iglesias, D.; Marchesan, S.; Laganà, A. New magnetic graphitized carbon black TiO2 composite for phosphopeptide selective enrichment in shotgun phosphoproteomics. Anal. Chem. 2016, 88, 12043-12050.
[36]
La Barbera, G.; Capriotti, A. L.; Cavaliere, C.; Ferraris, F.; Montone, C. M.; Piovesana, S.; Zenezini Chiozzi, R.; Laganà, A. Saliva as a source of new phosphopeptide biomarkers: Development of a comprehensive analytical method based on shotgun peptidomics. Talanta 2018, 183, 245-249.
[37]
Li, X. S.; Zhu, G. T.; Luo, Y. B.; Yuan, B. F.; Feng, Y. Q. Synthesis and applications of functionalized magnetic materials in sample preparation. TrAC Trends Anal. Chem. 2013, 45, 233-247.
[38]
Papi, M.; Palmieri, V.; Digiacomo, L.; Giulimondi, F.; Palchetti, S.; Ciasca, G.; Perini, G.; Caputo, D.; Cartillone, M. C.; Cascone, C. et al. Converting the personalized biomolecular corona of graphene oxide nanoflakes into a high-throughput diagnostic test for early cancer detection. Nanoscale 2019, 11, 15339-15346.
[39]
Grimme, S.; Bannwarth, C.; Shushkov, P. A robust and accurate tight-binding quantum chemical method for structures, vibrational frequencies, and noncovalent interactions of large molecular systems parametrized for all spd-block elements (Z = 1-86). J. Chem. Theory Comput. 2017, 13, 1989-2009.
[40]
Bannwarth, C.; Ehlert, S.; Grimme, S. GFN2-xTB—an accurate and broadly parametrized self-consistent tight-binding quantum chemical method with multipole electrostatics and density-dependent dispersion contributions. J. Chem. Theory Comput. 2019, 15, 1652-1671.
[41]
Gebhardt, P.; Pattinson, S. W.; Ren, Z. B.; Cooke, D. J.; Elliott, J. A.; Eder, D. Crystal engineering of zeolites with graphene. Nanoscale 2014, 6, 7319-7324.
[42]
Martins, P. M.; Ferreira, C. G.; Silva, A. R.; Magalhães, B.; Alves, M. M.; Pereira, L.; Marques, P. A. A. P.; Melle-Franco, M.; Lanceros-Méndez, S. TiO2/graphene and TiO2/graphene oxide nanocomposites for photocatalytic applications: A computer modeling and experimental study. Compos. Part B: Eng. 2018, 145, 39-46.
[43]
Hamad, S.; Catlow, C. R. A.; Woodley, S. M.; Lago, S.; Mejías, J. A. Structure and stability of small TiO2 nanoparticles. J. Phys. Chem. B 2005, 109, 15741-15748.
[44]
Sharma, K.; D’Souza, R. C. J.; Tyanova, S.; Schaab, C.; Wiśniewski, J. R.; Cox, J.; Mann, M. Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Rep. 2014, 8, 1583-1594.
[45]
Solari, F. A.; Dell’Aica, M.; Sickmann, A.; Zahedi, R. P. Why phosphoproteomics is still a challenge. Mol. Biosyst. 2015, 11, 1487-1493.
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Publication history
Copyright
Acknowledgements

Publication history

Received: 30 September 2019
Revised: 15 December 2019
Accepted: 21 December 2019
Published: 03 January 2020
Issue date: February 2020

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2020

Acknowledgements

This work was supported by PRIN 2015, project number 2015TWP83Z. The authors would like to acknowledge networking support by the COST Action MultiComp CA15107, as well as financial support from the Slovenian Research Agency (ARRS) for research core funding No. (P2-0089) and projects No. (J1-7302 and J3-7494).

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