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Biocompatibility of nitrogen-doped multiwalled carbon nanotubes with murine fibroblasts and human hematopoietic stem cells

  • Jose G. Munguia-Lopez
  • Rodrigo Juarez
  • Emilio Muñoz-Sandoval
  • Marco A. Kalixto-Sanchez
  • Joseph Matthew Kinsella
  • Antonio De Leon-RodriguezEmail author
Research Paper
  • 89 Downloads

Abstract

Chemical vapor deposition (CVD) methods to create carbon nanotubes (CNTs) with specific dopant atoms have been of interest in biomedical applications due to the relative ease of synthesis of doped CNTs with controlled physical properties. However, CNTs generated from CVD are often heterogeneous in chemical functionality, size, aspect ratio, number of walls, and conducting properties resulting in potential inconsistencies during measurement of the physiological activity of cell-CNT interactions. In this work, the biocompatibility of nitrogen-doped multiwalled carbon nanotubes (CNx) with both murine fibroblasts and human hematopoietic stem cells (hHSC) was evaluated. CNx were synthesized by CVD, purified, characterized, and classified into three fractions designated as small-CNx (S-CNx), medium (M-CNx), and large (L-CNx). Mammalian cells were incubated with CNx doses between 0.07 and 70 μg/mL, and cell viability was evaluated. hHSC and murine fibroblast both demonstrated non-significant differences in proliferation rates when exposed to M-CN, whereas, either cells experienced inhibited growth following exposure to either S-CNx and L-CNx under the same conditions. In this work, it has been demonstrated that CNTs produced by CVD have differences on the biocompatibility with mammalian cells, but the M-CNx could be a great candidate for biomedical applications.

Keywords

Nanomaterials Nitrogen-doped carbon nanotubes Murine cells Stem cells Biomedical applications 

Notes

Acknowledgments

The authors thank L. Aldana and Abdullah Chaudhary for the English review and V. Balderas for his technical assistance.

Funding

This research was funded by The Marcos Moshinsky Foundation and CONACYT-Mexico grant number CB-2013-220744 and 250279.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11051_2019_4637_MOESM1_ESM.docx (294 kb)
ESM 1 (DOCX 293 kb)

References

  1. Andrade-Zaldívar H, Kalixto-Sánchez MA, de la Rosa APB, De León-Rodríguez A (2011) Expansion of human hematopoietic cells from umbilical cord blood using roller bottles in CO2 and CO2-free atmosphere. Stem Cells Dev 20:593–598.  https://doi.org/10.1089/scd.2010.0236 CrossRefGoogle Scholar
  2. Bari S et al (2013) Protective role of functionalized single walled carbon nanotubes enhance ex vivo expansion of hematopoietic stem and progenitor cells in human umbilical cord blood nanomedicine. Nanotechnol Biol Med 9:1304–1316.  https://doi.org/10.1016/j.nano.2013.05.009 CrossRefGoogle Scholar
  3. Bari S et al (2015) Mitochondrial superoxide reduction and cytokine secretion skewing by carbon nanotube scaffolds enhance ex vivo expansion of human cord blood hematopoietic progenitors nanomedicine. Nanotechnol Biol Med 11:1643–1656.  https://doi.org/10.1016/j.nano.2015.06.005 CrossRefGoogle Scholar
  4. Bazargan A, McKay G (2012) A review – Synthesis of carbon nanotubes from plastic wastes. Chem Eng J 195-196:377–391.  https://doi.org/10.1016/j.cej.2012.03.077 CrossRefGoogle Scholar
  5. Blazer-Yost BL et al (2011) Effect of carbon nanoparticles on renal epithelial cell structure, barrier function, and protein expression. Nanotoxicology 5:354–371.  https://doi.org/10.3109/17435390.2010.514076 CrossRefGoogle Scholar
  6. Canapè C, Foillard S, Bonafè R, Maiocchi A, Doris E (2015) Comparative assessment of the in vitro toxicity of some functionalized carbon nanotubes and fullerenes. RSC Adv 5:68446–68453.  https://doi.org/10.1039/c5ra11489f CrossRefGoogle Scholar
  7. Canavan HE, Cheng X, Graham DJ, Ratner BD, Castner DG (2005) Cell sheet detachment affects the extracellular matrix: a surface science study comparing thermal liftoff, enzymatic, and mechanical methods. J Biomed Mater Res Part A 75A:1–13.  https://doi.org/10.1002/jbm.a.30297 CrossRefGoogle Scholar
  8. Carrero-Sanchez JC, Elias AL, Mancilla R, Arrellin G, Terrones H, Laclette JP, Terrones M (2006) Biocompatibility and toxicological studies of carbon nanotubes doped with nitrogen. Nano Lett 6:1609–1616.  https://doi.org/10.1021/nl060548p CrossRefGoogle Scholar
  9. Cui HF, Vashist SK, Al-Rubeaan K, Luong JH, Sheu FS (2010) Interfacing carbon nanotubes with living mammalian cells and cytotoxicity issues. Chem Res Toxicol 23:1131–1147.  https://doi.org/10.1021/tx100050h CrossRefGoogle Scholar
  10. Cui X, Wan B, Yang Y, Ren X, Guo LH (2017) Length effects on the dynamic process of cellular uptake and exocytosis of single-walled carbon nanotubes in murine macrophage cells. Sci Rep 7:1518.  https://doi.org/10.1038/s41598-017-01746-9 CrossRefGoogle Scholar
  11. De Volder MF, Tawfick SH, Baughman RH, Hart AJ (2013) Carbon nanotubes: present and future commercial applications. Science 339:535–539.  https://doi.org/10.1126/science.1222453 CrossRefGoogle Scholar
  12. Escobar Barrios VA, Rangel Méndez JR, Pérez Aguilar NV, Andrade Espinosa G, Dávila Rodríguez JL (2012) FTIR - an essential characterization technique for polymeric materials. In: Theophanides T (ed) Infrared Spectroscopy. IntechOpen.  https://doi.org/10.5772/36044 Google Scholar
  13. Ferreira L, Karp JM, Nobre L, Langer R (2008) New opportunities: the use of nanotechnologies to manipulate and track stem cells. Cell Stem Cell 3:136–146.  https://doi.org/10.1016/j.stem.2008.07.020 CrossRefGoogle Scholar
  14. Fisher C, Rider AE, Jun Han Z, Kumar S, Levchenko I, Ostrikov K (2012) Applications and nanotoxicity of carbon nanotubes and graphene in biomedicine. J Nanomater 2012:1–19.  https://doi.org/10.1155/2012/315185 CrossRefGoogle Scholar
  15. He S et al (2017) Biocompatible carbon nanotube fibers for implantable supercapacitors. Carbon 122:162–167.  https://doi.org/10.1016/j.carbon.2017.06.053 CrossRefGoogle Scholar
  16. Hirata E, Akasaka T, Uo M, Takita H, Watari F, Yokoyama A (2012) Carbon nanotube-coating accelerated cell adhesion and proliferation on poly (L-lactide). Appl Surf Sci 262:24–27.  https://doi.org/10.1016/j.apsusc.2012.01.012 CrossRefGoogle Scholar
  17. Huang L, Liu M, Huang H, Wen Y, Zhang X, Wei Y (2018) Recent advances and progress on melanin-like materials and their biomedical applications. Biomacromolecules 19:1858–1868.  https://doi.org/10.1021/acs.biomac.8b00437 CrossRefGoogle Scholar
  18. Jiang K, Eitan A, Schadler LS, Ajayan PM, Siegel RW, Grobert N, Mayne M, Reyes-Reyes M, Terrones H, Terrones M (2003) Selective attachment of gold nanoparticles to nitrogen-doped carbon nanotubes. Nano Lett 3:275–277.  https://doi.org/10.1021/nl025914t CrossRefGoogle Scholar
  19. Jourdain V, Bichara C (2013) Current understanding of the growth of carbon nanotubes in catalytic chemical vapour deposition. Carbon 58:2–39.  https://doi.org/10.1016/j.carbon.2013.02.046 CrossRefGoogle Scholar
  20. Kaiser JP, Buerki-Thurnherr T, Wick P (2013) Influence of single walled carbon nanotubes at subtoxical concentrations on cell adhesion and other cell parameters of human epithelial cells Journal of King Saud University. Science 25:15–27.  https://doi.org/10.1016/j.jksus.2012.06.003 CrossRefGoogle Scholar
  21. Kamalakaran R et al (2000) Synthesis of thick and crystalline nanotube arrays by spray pyrolysis. Appl Phys Lett 77:3385–3387CrossRefGoogle Scholar
  22. Kim AD, Stachura DL, Traver D (2014) Cell signaling pathways involved in hematopoietic stem cell specification. Exp Cell Res 329:227–233.  https://doi.org/10.1016/j.yexcr.2014.10.011 CrossRefGoogle Scholar
  23. Krenning G, Zeisberg EM, Kalluri R (2010) The origin of fibroblasts and mechanism of cardiac fibrosis. J Cell Physiol 225:631–637.  https://doi.org/10.1002/jcp.22322 CrossRefGoogle Scholar
  24. Kunzmann A, Andersson B, Thurnherr T, Krug H, Scheynius A, Fadeel B (2011) Toxicology of engineered nanomaterials: focus on biocompatibility, biodistribution and biodegradation. Biochimica et Biophysica Acta (BBA) - general subjects 1810:361–373.  https://doi.org/10.1016/j.bbagen.2010.04.007 CrossRefGoogle Scholar
  25. Lanone S, Andujar P, Kermanizadeh A, Boczkowski J (2013) Determinants of carbon nanotube toxicity. Adv drug Deliv Rev.  https://doi.org/10.1016/j.addr.2013.07.019 CrossRefGoogle Scholar
  26. Li DJ, Niu LF (2003) Influence of N atomic percentages on cell attachment for CNx coatings. Bull Mater Sci 26:371–375.  https://doi.org/10.1007/BF02711178 CrossRefGoogle Scholar
  27. Li L, Lin R, He H, Sun M, Jiang L, Gao M (2014) Interaction of amidated single-walled carbon nanotubes with protein by multiple spectroscopic methods. J Lumin 145:125–131.  https://doi.org/10.1016/j.jlumin.2013.07.008 CrossRefGoogle Scholar
  28. Liao L, Pan C (2011) Enhanced electrochemical capacitance of nitrogen-doped carbon nanotubes synthesized from amine flames soft. Nanoscience Lett 01:16–23.  https://doi.org/10.4236/snl.2011.11004 CrossRefGoogle Scholar
  29. Lim WF, Inoue-Yokoo T, Tan KS, Lai MI, Sugiyama D (2013) Hematopoietic cell differentiation from embryonic and induced pluripotent stem cell. Stem Cell Res Ther 4:71Google Scholar
  30. Liu Y, Zhao Y, Sun B, Chen C (2013) Understanding the toxicity of carbon nanotubes. Acc Chem Res 46:702–713. doi.org/10.1021/ar300028m CrossRefGoogle Scholar
  31. Liu Z et al (2014) Carboxylation of multiwalled carbon nanotube enhanced its biocompatibility with L02 cells through decreased activation of mitochondrial apoptotic pathway. J Biomed Mater Res Part A 102:665–673.  https://doi.org/10.1002/jbm.a.34729 CrossRefGoogle Scholar
  32. Liu M et al (2015) Self-polymerization of dopamine and polyethyleneimine: novel fluorescent organic nanoprobes for biological imaging applications. J Mater Chem B 3:3476–3482.  https://doi.org/10.1039/c4tb02067g CrossRefGoogle Scholar
  33. Liu M, Zeng G, Wang K, Wan Q, Tao L, Zhang X, Wei Y (2016a) Recent developments in polydopamine: an emerging soft matter for surface modification and biomedical applications. Nanoscale 8:16819–16840.  https://doi.org/10.1039/c5nr09078d CrossRefGoogle Scholar
  34. Liu Z, Liu Y, Peng D (2016b) Hydroxylation of multi-walled carbon nanotubes: enhanced biocompatibility through reduction of oxidative stress initiated cell membrane damage, cell cycle arrestment and extrinsic apoptotic pathway. Environ Toxicol Pharmacol 47:124–130.  https://doi.org/10.1016/j.etap.2016.09.013 CrossRefGoogle Scholar
  35. Matsuoka M, Akasaka T, Totsuka Y, Watari F (2010) Strong adhesion of Saos-2 cells to multi-walled carbon nanotubes. Mater Sci Eng: B 173:182–186.  https://doi.org/10.1016/j.mseb.2009.12.044 CrossRefGoogle Scholar
  36. McAnulty RJ (2007) Fibroblasts and myofibroblasts: their source, function and role in disease. Int J Biochem Cell Biol 39:666–671.  https://doi.org/10.1016/j.biocel.2006.11.005 CrossRefGoogle Scholar
  37. Meng J, Song L, Xu H, Kong H, Wang C, Guo X, Xie S (2005) Effects of single-walled carbon nanotubes on the functions of plasma proteins and potentials in vascular prostheses. Nanomed : Nanotechnol Biol Med 1:136–142.  https://doi.org/10.1016/j.nano.2005.03.003 CrossRefGoogle Scholar
  38. Meysami SS, Dillon F, Koós AA, Aslam Z, Grobert N (2013a) Aerosol-assisted chemical vapour deposition synthesis of multi-wall carbon nanotubes: I mapping the reactor. Carbon 58:151–158.  https://doi.org/10.1016/j.carbon.2013.02.044 CrossRefGoogle Scholar
  39. Meysami SS, Koós AA, Dillon F, Grobert N (2013b) Aerosol-assisted chemical vapour deposition synthesis of multi-wall carbon nanotubes: II an analytical study. Carbon 58:159–169.  https://doi.org/10.1016/j.carbon.2013.02.041 CrossRefGoogle Scholar
  40. Mihalchik AL et al (2015) Effects of nitrogen-doped multi-walled carbon nanotubes compared to pristine multi-walled carbon nanotubes on human small airway epithelial cells. Toxicology.  https://doi.org/10.1016/j.tox.2015.03.008 CrossRefGoogle Scholar
  41. Mubarak NM, Abdullah EC, Jayakumar NS, Sahu JN (2014) An overview on methods for the production of carbon nanotubes. J Ind Eng Chem 20:1186–1197.  https://doi.org/10.1016/j.jiec.2013.09.001 CrossRefGoogle Scholar
  42. Mundra RV, Wu X, Sauer J, Dordick JS, Kane RS (2014) Nanotubes in biological applications. Curr Opin Biotechnol 28:25–32.  https://doi.org/10.1016/j.copbio.2013.10.012 CrossRefGoogle Scholar
  43. Munguía-Lopez JG, Muñoz-Sandoval E, Ortiz-Medina J, Rodriguez-Macias FJ, De Leon-Rodriguez A (2015) Effects of nitrogen-doped multiwall carbon nanotubes on murine fibroblasts. J Nanomater 2015:1–7.  https://doi.org/10.1155/2015/801606 CrossRefGoogle Scholar
  44. Muñoz-Sandoval E, Fajardo-Díaz JL, Sánchez-Salas R, Cortés-López AJ, López-Urías F (2018) Two sprayer CVD synthesis of nitrogen-doped carbon sponge-type nanomaterials. Sci Rep 8:2983.  https://doi.org/10.1038/s41598-018-20079-9 CrossRefGoogle Scholar
  45. Nxumalo EN, Nyamori VO, Coville NJ (2008) CVD synthesis of nitrogen doped carbon nanotubes using ferrocene/aniline mixtures. J Organomet Chem 693:2942–2948.  https://doi.org/10.1016/j.jorganchem.2008.06.015 CrossRefGoogle Scholar
  46. Pulskamp K, Diabate S, Krug HF (2007) Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol Lett 168:58–74.  https://doi.org/10.1016/j.toxlet.2006.11.001 CrossRefGoogle Scholar
  47. Ryabenko AG, Dorofeeva TV, Zvereva GI (2004) UV–VIS–NIR spectroscopy study of sensitivity of single-wall carbon nanotubes to chemical processing and Van-der-Waals SWNT/SWNT interaction. Verification of the SWNT content measurements by absorption. Spectrosc Carbon 42:1523–1535.  https://doi.org/10.1016/j.carbon.2004.02.005 CrossRefGoogle Scholar
  48. Ryoo SR, Kim YK, Kim MH, Min DH (2010) Behaviors of NIH-3T3 fibroblasts on graphene/carbon nanotubes: proliferation, focal adhesion, and gene transfection studies. ACS Nano 4:6587–6598.  https://doi.org/10.1021/nn1018279 CrossRefGoogle Scholar
  49. Sabuncu AC, Kalluri BS, Qian S, Stacey MW, Beskok A (2010) Dispersion state and toxicity of mwCNTs in cell culture medium with different T80 concentrations. Colloids Surf B: Biointerfaces 78:36–43.  https://doi.org/10.1016/j.colsurfb.2010.02.005 CrossRefGoogle Scholar
  50. Sanchez-Salas R (2015) Sintesis de nanotubos de carbono dopados con nitrogeno: un estudio sistemático. Instituto Potosino de Investigación Científica y Tecnológica, A.C (IPICyT)Google Scholar
  51. Shah KA, Tali BA (2016) Synthesis of carbon nanotubes by catalytic chemical vapour deposition: a review on carbon sources, catalysts and substrates. Mater Sci Semicond Process 41:67–82.  https://doi.org/10.1016/j.mssp.2015.08.013 CrossRefGoogle Scholar
  52. Shi Y et al (2017) Biomimetic PEGylation of carbon nanotubes through surface-initiated RAFT polymerization. Mater Sci Eng C Mater Biol Appl 80:404–410.  https://doi.org/10.1016/j.msec.2017.06.009 CrossRefGoogle Scholar
  53. Sohaebuddin SK, Thevenot PT, Baker D, Eaton JW, Tang L (2010) Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol 7:22.  https://doi.org/10.1186/1743-8977-7-22 CrossRefGoogle Scholar
  54. Tucureanu V, Matei A, Avram AM (2016) FTIR Spectroscopy for Carbon Family Study. Crit Rev Anal Chem 46:502–520.  https://doi.org/10.1080/10408347.2016.1157013 CrossRefGoogle Scholar
  55. Weissleder R (2001) A clearer vision for in vivo imaging. Nat Biotechnol 19:316–317.  https://doi.org/10.1038/86684 CrossRefGoogle Scholar
  56. Wu X, Tao Y, Lu Y, Dong L, Hu Z (2006) High-pressure pyrolysis of melamine route to nitrogen-doped conical hollow and bamboo-like carbon nanotubes. Diam Relat Mater 15:164–170.  https://doi.org/10.1016/j.diamond.2005.09.018 CrossRefGoogle Scholar
  57. Xiao H et al (2012) Photodynamic effects of chlorin e6 attached to single wall carbon nanotubes through noncovalent interactions. Carbon 50:1681–1689.  https://doi.org/10.1016/j.carbon.2011.12.013 CrossRefGoogle Scholar
  58. Zhang X et al (2010) Biodistribution and toxicity of nanodiamonds in mice after intratracheal instillation. Toxicol Lett 198:237–243.  https://doi.org/10.1016/j.toxlet.2010.07.001 CrossRefGoogle Scholar
  59. Zhang X et al (2011a) Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration. Carbon 49:986–995.  https://doi.org/10.1016/j.carbon.2010.11.005 CrossRefGoogle Scholar
  60. Zhang X, Zhu Y, Li J, Zhu Z, Li J, Li W, Huang Q (2011b) Tuning the cellular uptake and cytotoxicity of carbon nanotubes by surface hydroxylation. J Nanopart Res 13:6941–6952.  https://doi.org/10.1007/s11051-011-0603-9 CrossRefGoogle Scholar
  61. Zhang M, Zhou X, Iijima S, Yudasaka M (2012a) Small-sized carbon nanohorns enabling cellular uptake control. Small 8:2524–2531.  https://doi.org/10.1002/smll.201102595 CrossRefGoogle Scholar
  62. Zhang X, Hu W, Li J, Tao L, Wei Y (2012b) A comparative study of cellular uptake and cytotoxicity of multi-walled carbon nanotubes, graphene oxide, and nanodiamond. Toxicol Res 1:1.  https://doi.org/10.1039/c2tx20006f CrossRefGoogle Scholar
  63. Zhang X et al (2012c) Biocompatible polydopamine fluorescent organic nanoparticles: facile preparation and cell imaging. Nanoscale 4:5581–5584.  https://doi.org/10.1039/c2nr31281f CrossRefGoogle Scholar
  64. Zhang X et al (2015) Interaction of tannic acid with carbon nanotubes: enhancement of dispersibility and biocompatibility. Toxicol Res 4:160–168.  https://doi.org/10.1039/c4tx00066h CrossRefGoogle Scholar
  65. Zhang X, Huang Q, Deng F, Huang H, Wan Q, Liu M, Wei Y (2017) Mussel-inspired fabrication of functional materials and their environmental applications: Progress and prospects. Appl Mater Today 7:222–238.  https://doi.org/10.1016/j.apmt.2017.04.001 CrossRefGoogle Scholar
  66. Zhang M et al (2018) Size-dependent cell uptake of carbon nanotubes by macrophages: a comparative and quantitative study. Carbon 127:93–101.  https://doi.org/10.1016/j.carbon.2017.10.085 CrossRefGoogle Scholar
  67. Zhao X, Liu R (2012) Recent progress and perspectives on the toxicity of carbon nanotubes at organism, organ, cell, and biomacromolecule levels. Environ Int 40:244–255.  https://doi.org/10.1016/j.envint.2011.12.003 CrossRefGoogle Scholar
  68. Zhao F, Zhao Y, Liu Y, Chang X, Chen C, Zhao Y (2011a) Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small 7:1322–1337.  https://doi.org/10.1002/smll.201100001 CrossRefGoogle Scholar
  69. Zhao ML, Li DJ, Yuan L, Yue YC, Liu H, Sun X (2011b) Differences in cytocompatibility and hemocompatibility between carbon nanotubes and nitrogen-doped carbon nanotubes. Carbon 49:3125–3133.  https://doi.org/10.1016/j.carbon.2011.03.037 CrossRefGoogle Scholar
  70. Zhou L, Forman HJ, Ge Y, Lunec J (2017) Multi-walled carbon nanotubes: a cytotoxicity study in relation to functionalization, dose and dispersion. Toxicol in vitro 42:292–298.  https://doi.org/10.1016/j.tiv.2017.04.027 CrossRefGoogle Scholar
  71. Zhu Y, Li W, Li Q, Li Y, Li Y, Zhang X, Huang Q (2009) Effects of serum proteins on intracellular uptake and cytotoxicity of carbon nanoparticles. Carbon 47:1351–1358.  https://doi.org/10.1016/j.carbon.2009.01.026 CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Molecular BiologyInstituto Potosino de Investigación Científica y Tecnológica, A.C. San Luis PotosíMexico
  2. 2.Department of BioengineeringMcGill UniversityMontrealCanada
  3. 3.Advanced Materials DepartmentInstituto Potosino de Investigación Científica y Tecnológica, A.C. San Luis PotosíMexico
  4. 4.Hospital General del ISSSTESan Luis PotosiMexico

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