Rheological Properties of Different Graphene Nanomaterials in Biological Media

  1. Cerpa-Naranjo, Arisbel 2
  2. Pérez-Piñeiro, Javier 2
  3. Navajas-Chocarro, Pablo 2
  4. Arce, Mariana P. 2
  5. Lado-Touriño, Isabel 2
  6. Barrios-Bermúdez, Niurka 2
  7. Moreno, Rodrigo 1
  8. Rojas-Cervantes, María Luisa 3
  1. 1 Instituto de Cerámica y Vidrio
    info

    Instituto de Cerámica y Vidrio

    Madrid, España

    ROR https://ror.org/02h7vfp25

  2. 2 Universidad Europea de Madrid
    info

    Universidad Europea de Madrid

    Madrid, España

    ROR https://ror.org/04dp46240

  3. 3 Universidad Nacional de Educación a Distancia
    info

    Universidad Nacional de Educación a Distancia

    Madrid, España

    ROR https://ror.org/02msb5n36

Erakutsi afiliazioak +
Aldizkaria:
Materials

ISSN: 1996-1944

Argitalpen urtea: 2022

Alea: 15

Zenbakia: 10

Orrialdeak: 3593

Mota: Artikulua

DOI: 10.3390/MA15103593 GOOGLE SCHOLAR lock_openSarbide irekia editor

Beste argitalpen batzuk: Materials

Laburpena

Carbon nanomaterials have received increased attention in the last few years due to their potential applications in several areas. In medicine, for example, these nanomaterials could be used as contrast agents, drug transporters, and tissue regenerators or in gene therapy. This makes it necessary to know the behavior of carbon nanomaterials in biological media to assure good fluidity and the absence of deleterious effects on human health. In this work, the rheological characterization of different graphene nanomaterials in fetal bovine serum and other fluids, such as bovine serum albumin and water, is studied using rotational and microfluidic chip rheometry. Graphene oxide, graphene nanoplatelets, and expanded graphene oxide at concentrations between 1 and 3 mg/mL and temperatures in the 25–40 °C range were used. The suspensions were also characterized by transmission and scanning electron microscopy and atomic force microscopy, and the results show a high tendency to aggregation and reveals that there is a protein–nanomaterial interaction. Although rotational rheometry is customarily used, it cannot provide reliable measurements in low viscosity samples, showing an apparent shear thickening, whereas capillary viscometers need transparent samples; therefore, microfluidic technology appears to be a suitable method to measure low viscosity, non-transparent Newtonian fluids, as it is able to determine small variations in viscosity. No significant changes in viscosity are found within the solid concentration range studied but it decreases between 1.1 and 0.6 mPa·s when the temperature raises from 25 to 40 °C.

€ Ikusi finantzaketa

Finantzaketari buruzko informazioa

Finantzatzaile

Erreferentzia bibliografikoak

  • 1. Novoselov, K.S.; Geim, A.K.; Morozov, S.V.; Jiang, D.; Zhang, Y.; Dubonos, S.V.; Grigorieva, I.V.; Firsov, A.A. Electric field effect in atomically thin carbon films. Science 2004, 306, 666–669. [CrossRef] [PubMed]
  • 2. Yang, Y.; Asiri, A.M.; Tang, Z.; Du, D.; Lin, Y. Graphene based materials for biomedical applications. Mater. Today 2013, 16, 365–373. [CrossRef]
  • 3. Mkhoyan, K.A.; Contryman, A.W.; Silcox, J.; Stewart, D.A.; Eda, G.; Mattevi, C.; Miller, S.; Chhowalla, M. Atomic and electronic structure of graphene-oxide. Nanoletters 2009, 9, 1058–1063. [CrossRef]
  • 4. Zhang, L.; Xia, J.; Zhao, Q.; Liu, L.; Zhang, Z. Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs. Small 2010, 6, 537–544. [CrossRef] [PubMed]
  • 5. Yin, D.; Li, Y.; Lin, H.; Guo, B.; Du, Y.; Li, X.; Jia, H.; Zhao, X.; Tang, J.; Zhang, L. Functional graphene oxide as a plasmid-based Stat3 siRNA carrier inhibits mouse malignant melanoma growth in vivo. Nanotechnology 2013, 24, 105102. [CrossRef] [PubMed]
  • 6. Bolibok, P.; Szymczak, B.; Roszek, K.; Terzyk, A.P.; Wisniewski, M. A new approach to obtaining nano-sized graphene oxide for biomedical applications. Materials 2021, 14, 1327. [CrossRef]
  • 7. Matalkah, F.; Soroushian, P. Graphene nanoplatelet for enhancement the mechanical properties and durability characteristics of alkali activated binder. Constr. Build. Mater. 2020, 249, 118773. [CrossRef]
  • 8. Cho, J.; Lee, H.; Nam, K.H.; Yeo, H.; Yang, C.M.; Seong, D.G.; Lee, D.; Kim, S.Y. Enhanced electrical conductivity of polymer nanocomposite based on edge-selectivity functionalized graphene nanoplatelets. Compos. Sci. Technol. 2020, 189, 108001. [CrossRef]
  • 9. Park, C.S.; Yoon, H.; Kwon, O.S. Graphene-based nanoelectronic biosensors. J. Ind. Eng. Chem. 2016, 38, 13–22. [CrossRef]
  • 10. Kargar, S.; Elhamifar, D.; Zarnegaryan, A. Ionic liquid modified graphene oxide supported Mo-complex: A novel, efficient and highly stable catalyst. Surf. Interfaces 2021, 23, 100946. [CrossRef]
  • 11. Liu, S.; Zeng, T.H.; Hofmann, M.; Burcombe, E.; Wei, J.; Jiang, R.; Kong, J.; Chen, Y. Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: Membrane and oxidative stress. ACS Nano 2011, 5, 6971–6980. [CrossRef] [PubMed]
  • 12. Kuropka, P.; Dobrzynski, M.; Bazanow, B.; Stygar, D.; Gebarowski, T.; Leskow, A.; Tarnowska, M.; Szyszka, K.; Malecka, M.; Nowak, N.; et al. A Study of the Impact of Graphene Oxide on Viral Infection Related to A549 and TC28a2 Human Cell Lines. Materials 2021, 14, 7788. [CrossRef] [PubMed]
  • 13. Bhattacharya, K.; Mukherjee, S.P.; Gallud, A.; Burkert, S.C.; Bistarelli, S.; Bellucci, S.; Bottini, M.; Star, A.; Fadeel, B. Biological interactions of carbon-based nanomaterials: From coronation to degradation. Nanomed. Nanotechnol. Biol. Med. 2016, 12, 333–351. [CrossRef] [PubMed]
  • 14. Chen, C.; Xi, Y.; Weng, Y. Progress in the Development of Graphene-Based Biomaterials for Tissue Engineering and Regeneration. Materials 2022, 15, 2164. [CrossRef]
  • 15. Trusek, A.; Kijak, E. Drug Carriers Based on Graphene Oxide and Hydrogel: Opportunities and Challenges in Infection Control Tested by Amoxicillin Release. Materials 2021, 14, 3182. [CrossRef]
  • 16. Singh, D.P.; Herrera, C.E.; Singh, B.; Shing, S.; Shing, R.K.; Kumar, R. Graphene oxide: An efficient material and recent approach for biotechnological and biomedical applications. Mater. Sci. Eng. C 2018, 86, 173–197. [CrossRef]
  • 17. Kopac, T. Protein corona, understanding the nanoparticle-protein interactions and future perspectives: A critical review. Int. J. Biol. Macromol. 2021, 169, 290–301. [CrossRef]
  • 18. Sopotnik, M.; Leonardi, A.; Krizaj, I.; Dusak, P.; Makovec, D.; Mesaric, T.; Ulrih, N.P.; Junkar, I.; Sepcic, K.; Drobne, D. Comparative study of serum protein binding to three different carbon-based nanomaterials. Carbon 2015, 95, 560–572. [CrossRef]
  • 19. Mahmoudi, M.; Lynch, I.; Ejtehadi, M.R.; Monopoli, M.P.; Bombelli, F.B.; Laurent, S. Protein-nanoparticle interactions: Opportunities and challenges. Chem. Rev. 2011, 111, 5610–5637. [CrossRef]
  • 20. Wu, Z.; Zhang, B.; Yan, B. Regulation of enzyme activity through interactions with nanoparticles. Int. J. Mol. Sci. 2009, 10, 4198–4209. [CrossRef]
  • 21. Sheng, A.; Liu, F.; Xie, N.; Liu, J. Impact of proteins on aggregation kinetics and adsorption ability of hematite nanoparticles in aqueous dispersions. Environ. Sci. Technol. 2016, 50, 2228–2235. [CrossRef] [PubMed]
  • 22. Zhao, X.; Zou, X.; Ye, L. Controlled pH-and glucose-responsive drug release behavior of cationic chitosan based nano-composite hydrogels by using graphene oxide as drug nanocarrier. J. Ind. Eng. Chem. 2017, 49, 36–45. [CrossRef]
  • 23. Wu, C.; He, Q.; Zhu, A.; Yang, H.; Liu, Y. Probing the protein conformation and adsorption behaviors in nanographene oxide-protein complexes. J. Nanosci. Nanotechnol. 2014, 14, 2591–2598. [CrossRef] [PubMed]
  • 24. Moghassemi, S.; Hadjizadeh, A.; Omidfar, K. Formulation and Characterization of Bovine Serum Albumin-Loaded Niosome. AAPS PharmSciTech 2017, 18, 27–33. [CrossRef]
  • 25. Zheng, X.; Baker, H.; Hancock, W.S.; Fawaz, F.; McCaman, M.; Pungor, E., Jr. Proteomic analysis for the assessment of different lots of fetal bovine serum as a raw material for cell culture. Part IV. Application of proteomics to the manufacture of biological drugs. Biotechnol. Prog. 2006, 22, 1294–1300. [CrossRef]
  • 26. Punyiczki, M.; Rosenberg, A. The effect of viscosity on the accessibility of the single tryptophan in human serum albumin. Biophys. Chem. 1992, 42, 93–100. [CrossRef]
  • 27. Zidar, M.; Rozman, P.; Belko-Parkel, K.; Ravnik, M. Control of viscosity in biopharmaceutical protein formulations. J. Colloid Interface Sci. 2020, 580, 308–317. [CrossRef]
  • 28. Wonerow, T.; Uhler, M.; Nuppnau, J.; Kretzer, J.P.; Mantwill, F. Rheologic Behavior of Bovine Calf Serum. Materials 2021, 14, 2538. [CrossRef]
  • 29. Vallejo, J.P.; Gómez-Barreiro, S.; Cabaleiro, D.; Gracia-Fernández, C.; Fernández-Seara, J.; Lugo, L. Flow behaviour of suspensions of functionalized graphene nanoplatelets in propylene glycol–water mixtures. Int. Commun. Heat Mass Transf. 2018, 91, 150–157. [CrossRef]
  • 30. Alyamac, E.; Fidan, T.; Turgut, A.; Ozgur, M. Stability, rheology, and thermophysical properties of surfactant free aqueous single-walled carbon nanotubes and graphene nanoplatelets nanofluids: A comparative study. J. Dispers. Sci. Technol. 2021, 1–10. [CrossRef]
  • 31. Cerpa, A.; Lado, I.; Quiroga, O.; Moreno, R.; García, R.; Cerdán, S.; Abu-Lail, N.I. Colloidal and rheological characterization of SWCNT in biological media. Int. J. Smart Nano Mater. 2019, 10, 300–315. [CrossRef]
  • 32. Cerpa, A.; Ibañez, B.; Lado, I.; Arce, M.P.; Pérez, J.; Barrios, N.; Moreno, R.; Cerdán, S. Rheological behaviour of carbon nanotubes suspensions with biomedical applications. In Estudos em Biociencias e Biotecnologia, Chapter 2; Editora Artemis: Curitiba, Brazil, 2021; pp. 16–27.
  • 33. Lavin-Lopez, M.P.; Paton-Carrero, A.; Sanchez-Silva, L.; Valverde, J.L.; Romero, A. Influence of the reduction strategy in the synthesis of reduced graphene oxide. Adv. Powder Technol. 2017, 28, 3195–3203. [CrossRef]
  • 34. Lee, S.; Eom, S.H.; Chung, J.S.; Hur, S.H. Large-scale production of high-quality reduced graphene oxide. Chem. Eng. J. 2013, 233, 297–304. [CrossRef]
  • 35. Cheong, Y.K.; Arce, M.; Benito, A.; Chen, D.; Luengo, N.; Kerai, L.; Rodríguez, G.; Valverde, J.L.; Vadalia, M.; Cerpa, A.; et al. Synergistic antifungal study of PEGylated graphene oxides and copper nanoparticles against Candida albicans. Nanomaterials 2020, 10, 819. [CrossRef]
  • 36. Franqui, L.S.; De Farias, M.A.; Portugal, R.V.; Costa, C.A.; Domingues, R.R.; Souza-Filho, A.G.; Coluci, V.R.; Leme, A.F.P.; Martinez, D.S.T. Interaction of graphene oxide with cell culture medium: Evaluating the fetal bovine serum protein corona formation towards in vitro nanotoxicity assessment and nanobiointeractions. Mater. Sci. Eng. C 2019, 100, 363–377. [CrossRef]
  • 37. Zhu, Y.; Li, W.; Li, Q.; Li, Y.; Li, Y.; Zhang, X.; Huang, Q. Effects of serum proteins on intracellular uptake and cytotoxicity of carbon nanoparticles. Carbon 2009, 47, 1351–1358. [CrossRef]
  • 38. Park, M.; Nguyen, T.P.; Choi, K.S.; Park, J.; Ozturk, A.; Kim, S.Y. MoS2-nanosheet/graphene-oxide composite hole injection layer in organic light-emitting diodes. Electron. Mater. Lett. 2017, 13, 344–350. [CrossRef]
  • 39. Palmieri, V.; Bugli, F.; Cacaci, M.; Perini, G.; De Maio, F.; Delogu, G.; Torelli, R.; Conti, C.; Sanguinetti, M.; De Spirito, M.; et al. Graphene oxide coatings prevent Candida albicans biofilm formation with a controlled release of curcumin-loaded nanocomposites. Nanomedicine 2018, 13, 2867–2879. [CrossRef]
  • 40. Sapsford, K.E.; Tyner, K.M.; Dair, B.J.; Deschamps, J.R.; Medintz, I.L. Analyzing nanomaterial bioconjugates: A review of current and emerging purification and characterization techniques. Anal. Chem. 2011, 83, 4453–4488. [CrossRef]
  • 41. Carnicer, V.; Alcázar, C.; Orts, M.J.; Sánchez, E.; Moreno, R. Microfluidic rheology: A new approach to measure viscosity of ceramic suspensions at extremely high shear rates. Open Ceram. 2021, 5, 100052. [CrossRef]
  • 42. Raslan, A.; Saenz, L.; Espona-Noguera, A.; Ochoa, A.M.; Sanjuán, M.L.; Cañibano-Hernández, A.; Gálvez-Martín, P.; Ciriza, J.; Pedraz, J.L. BSA- and Elastin-coated GO, but no collagen-coated GO, enhance the biological performance of alginate hydrogels. Pharmaceutics 2020, 12, 543. [CrossRef] [PubMed]
  • 43. Gupta, S.; Wang, W.S.; Vanapalli, S.A. Microfluidic viscometers for shear rheology of complex fluids and biofluids. Biomicrofluidics 2016, 10, 043402. [CrossRef] [PubMed]
  • 44. Rothammer, B.; Marian, M.; Rummel, F.; Schroeder, S.; Uhler, M.; Kretzer, J.P.; Tremmel, S.; Wartzack, S. Rheological behavior of an artificial synovial fluid—Influence of temperature, shear rate and pressure. J. Mech. Behav. Biomed. Mater. 2021, 115, s104278. [CrossRef] [PubMed]
  • 45. Bortel, E.; Charbonnier, B.; Heuberger, R. Development of a Synthetic Synovial Fluid for Tribological Testing. Lubricants 2015, 3, 664–686. [CrossRef]
  • 46. Mazzucco, D.; McKinley, G.; Scott, R.D.; Spector, M. Rheology of joint fluid in total knee arthroplasty patients. J. Orthop. Res. 2002, 20, 1157–1163. [CrossRef]