Biomaterials Research (생체재료학회지)

Korean Society for Biomaterials (한국생체재료학회)
권호 표지
DOI QR코드

DOI QR Code

Application of black phosphorus nanodots to live cell imaging

  • Shin, Yong Cheol (Research Center for Energy Convergence Technology, Pusan National University) ;
  • Song, Su-Jin (Department of Cogno-Mechatronics Engineering, College of Nanoscience & Nanotechnology, Pusan National University) ;
  • Lee, Yu Bin (Department of Cogno-Mechatronics Engineering, College of Nanoscience & Nanotechnology, Pusan National University) ;
  • Kang, Moon Sung (Department of Cogno-Mechatronics Engineering, College of Nanoscience & Nanotechnology, Pusan National University) ;
  • Lee, Hyun Uk (Advanced Nano-Surface Research Group, Korea Basic Science Institute (KBSI)) ;
  • Oh, Jin-Woo (Department of Nanofusion Technology, College of Nanoscience & Nanotechnology, Pusan National University) ;
  • Han, Dong-Wook (Department of Cogno-Mechatronics Engineering, College of Nanoscience & Nanotechnology, Pusan National University)
  • Received : 2018.07.23
  • Accepted : 2018.09.25
  • Published : 2018.12.31
⟨ Previous Next ⟩

Abstract

Background: Black phosphorus (BP) has emerged as a novel class of nanomaterials owing to its unique optical and electronic properties. BP, a two-dimensional (2D) nanomaterial, is a structure where phosphorenes are stacked together in layers by van der Waals interactions. However, although BP nanodots have many advantages, their biosafety and biological effect have not yet been elucidated as compared to the other nanomaterials. Therefore, it is particularly important to assess the cytotoxicity of BP nanodots for exploring their potentials as novel biomaterials. Methods: BP nanodots were prepared by exfoliation with a modified ultrasonication-assisted solution method. The physicochemical properties of BP nanodots were characterized by transmission electron microscopy, dynamic light scattering, Raman spectroscopy, and X-ray diffractometry. In addition, the cytotoxicity of BP nanodots against C2C12 myoblasts was evaluated. Moreover, their cell imaging potential was investigated. Results: Herein, we concentrated on evaluating the cytotoxicity of BP nanodots and investigating their cell imaging potential. It was revealed that the BP nanodots were cytocompatible at a low concentration, although the cell viability was decreased with increasing BP nanodot concentration. Furthermore, our results demonstrated that the cells took up the BP nanodots, and the BP nanodots exhibited green fluorescence. Conclusions: In conclusion, our findings suggest that the BP nanodots have suitable biocompatibility, and are promising candidates as fluorescence probes for biomedical imaging applications.

Keywords

Acknowledgement

Supported by : National Research Foundation (NRF), Korea Health Industry Development Institute (KHIDI)

References

  1. Oliveira SF, Bisker G, Bakh NA, Gibbs SL, Landry MP, Strano MS. Protein functionalized carbon nanomaterials for biomedical applications. Carbon. 2015;95:767-79. https://doi.org/10.1016/j.carbon.2015.08.076
  2. Shin YC, Song S-J, Shin D-M, Oh J-W, Hong SW, Choi YS, et al. Nanocomposite scaffolds for myogenesis revisited: functionalization with carbon nanomaterials and spectroscopic analysis. Appl Spectrosc Rev. 2017;53(2-4):129-56.
  3. Shin YC, Song S-J, Hong SW, Jeong SJ, Chrzanowski W, Lee J-C, et al. Multifaceted biomedical applications of functional graphene nanomaterials to coated substrates, patterned arrays and hybrid scaffolds. Nanomaterials. 2017;7(11):369. https://doi.org/10.3390/nano7110369
  4. Yi G, Son J, Yoo J, Park C, Koo H. Application of click chemistry in nanoparticle modification and its targeted delivery. Biomater Res. 2018;22(1):13. https://doi.org/10.1186/s40824-018-0123-0
  5. Kang E-S, Kim D-S, Suhito IR, Lee W, Song I, Kim T-H. Two-dimensional material-based bionano platforms to control mesenchymal stem cell differentiation. Biomater Res. 2018;22(1):10. https://doi.org/10.1186/s40824-018-0120-3
  6. Lee HU, Park SY, Lee SC, Choi S, Seo S, Kim H, et al. Black phosphorus (BP) nanodots for potential biomedical applications. Small. 2016;12(2):214-9. https://doi.org/10.1002/smll.201502756
  7. Batmunkh M, Bat-Erdene M, Shapter JG. Phosphorene and phosphorenebased materials-prospects for future applications. Adv Mater. 2016;28(39):8586-617. https://doi.org/10.1002/adma.201602254
  8. Wang H, Yang X, Shao W, Chen S, Xie J, Zhang X, et al. Ultrathin black phosphorus nanosheets for efficient singlet oxygen generation. J Am Chem Soc. 2015;137(35):11376-82. https://doi.org/10.1021/jacs.5b06025
  9. Erande MB, Pawar MS, Late DJ. Humidity sensing and photodetection behavior of electrochemically exfoliated atomically thin-layered black phosphorus nanosheets. ACS Appl Mater Interfaces. 2016;8(18):11548-56. https://doi.org/10.1021/acsami.5b10247
  10. Tao W, Zhu X, Yu X, Zeng X, Xiao Q, Zhang X, et al. Black phosphorus nanosheets as a robust delivery platform for cancer theranostics. Adv Mater. 2017;29(1):1603276. https://doi.org/10.1002/adma.201603276
  11. Tran V, Soklaski R, Liang Y, Yang L. Layer-controlled band gap and anisotropic excitons in few-layer black phosphorus. Phys Rev B. 2014;89(23):235319. https://doi.org/10.1103/PhysRevB.89.235319
  12. Woomer AH, Farnsworth TW, Hu J, Wells RA, Donley CL, Warren SC. Phosphorene: synthesis, scale-up, and quantitative optical spectroscopy. ACS Nano. 2015;9(9):8869-84. https://doi.org/10.1021/acsnano.5b02599
  13. Akahama Y, Endo S. Narita S-i. electrical properties of black phosphorus single crystals. J Phys Soc Jpn. 1983;52(6):2148-55. https://doi.org/10.1143/JPSJ.52.2148
  14. Morita A. Semiconducting black phosphorus. Appl Phys A Mater Sci Process. 1986;39(4):227-42. https://doi.org/10.1007/BF00617267
  15. Zhang J, Liu HJ, Cheng L, Wei J, Liang JH, Fan DD, et al. Phosphorene nanoribbon as a promising candidate for thermoelectric applications. Sci Rep. 2014;4:6452.
  16. Flores E, Ares JR, Castellanos-Gomez A, Barawi M, Ferrer IJ, Sanchez C. Thermoelectric power of bulk black-phosphorus. Appl Phys Lett. 2015;106(2):022102. https://doi.org/10.1063/1.4905636
  17. Cakir D, Sahin H, Peeters FM. Tuning of the electronic and optical properties of single-layer black phosphorus by strain. Phys Rev B. 2014;90(20):205421. https://doi.org/10.1103/PhysRevB.90.205421
  18. Hu T, Hashmi A, Hong J. Geometry, electronic structures and optical properties of phosphorus nanotubes. Nanotechnology. 2015;26(41):415702. https://doi.org/10.1088/0957-4484/26/41/415702
  19. Sun C, Wen L, Zeng J, Wang Y, Sun Q, Deng L, et al. One-pot solventless preparation of PEGylated black phosphorus nanoparticles for photoacoustic imaging and photothermal therapy of cancer. Biomaterials. 2016;91:81-9. https://doi.org/10.1016/j.biomaterials.2016.03.022
  20. Wei Q, Peng X. Superior mechanical flexibility of phosphorene and fewlayer black phosphorus. Appl Phys Lett. 2014;104(25):251915. https://doi.org/10.1063/1.4885215
  21. Jiang J-W, Park HS. Mechanical properties of single-layer black phosphorus. J Phys D Appl Phys. 2014;47(38):385304. https://doi.org/10.1088/0022-3727/47/38/385304
  22. Buscema M, Groenendijk DJ, Steele GA, van der HSJ Z, Castellanos-Gomez A. Photovoltaic effect in few-layer black phosphorus PN junctions defined by local electrostatic gating. Nat Commun. 2014;5:4651. https://doi.org/10.1038/ncomms5651
  23. Park CM, Sohn HJ. Black phosphorus and its composite for lithium rechargeable batteries. Adv Mater. 2007;19(18):2465-8. https://doi.org/10.1002/adma.200602592
  24. Xia F, Wang H, Jia Y. Rediscovering black phosphorus as an anisotropic layered material for optoelectronics and electronics. Nat Commun. 2014;5:4458. https://doi.org/10.1038/ncomms5458
  25. Wood JD, Wells SA, Jariwala D, Chen K-S, Cho E, Sangwan VK, et al. Effective passivation of exfoliated black phosphorus transistors against ambient degradation. Nano Lett. 2014;14(12):6964-70. https://doi.org/10.1021/nl5032293
  26. Saitoh Y, Terada N, Saitoh S, Ohno N, Jin T, Ohno S. Histochemical analyses and quantum dot imaging of microvascular blood flow with pulmonary edema in living mouse lungs by "in vivo cryotechnique". Histochem Cell Biol. 2012;137(2):137-51. https://doi.org/10.1007/s00418-011-0892-1
  27. Hainfeld JF, Smilowitz HM, O'Connor MJ, Dilmanian FA, Slatkin DN. Gold nanoparticle imaging and radiotherapy of brain tumors in mice. Nanomedicine. 2013;8(10):1601-9. https://doi.org/10.2217/nnm.12.165
  28. Bauer LM, Situ SF, Griswold MA, Samia ACS. High-performance iron oxide nanoparticles for magnetic particle imaging-guided hyperthermia (hMPI). Nanoscale. 2016;8(24):12162-9. https://doi.org/10.1039/C6NR01877G
  29. Tran VT, Kim J, Tufa LT, Oh S, Kwon J, Lee J. Magnetoplasmonic nanomaterials for biosensing/imaging and in vitro/in vivo biousability. Anal Chem. 2017;90(1):225-39. https://doi.org/10.1021/acs.analchem.7b04255
  30. Jeong Y, Na K. Synthesis of a gadolinium based-macrocyclic MRI contrast agent for effective cancer diagnosis. Biomater Res. 2018;22(1):17. https://doi.org/10.1186/s40824-018-0127-9
  31. Engel M, Steiner M, Avouris P. Black phosphorus photodetector for multispectral, high-resolution imaging. Nano Lett. 2014;14(11):6414-7. https://doi.org/10.1021/nl502928y
  32. Lu SB, Miao LL, Guo ZN, Qi X, Zhao CJ, Zhang H, et al. Broadband nonlinear optical response in multi-layer black phosphorus: an emerging infrared and mid-infrared optical material. Opt Express. 2015;23(9):11183-94. https://doi.org/10.1364/OE.23.011183
  33. Lee HU, Lee SC, Won J, Son B-C, Choi S, Kim Y, et al. Stable semiconductor black phosphorus (BP)@titanium dioxide ($TiO_{2}$) hybrid photocatalysts. Sci Rep. 2015;5:8691. https://doi.org/10.1038/srep08691
  34. Lee JH, Shin YC, Jin OS, Lee EJ, Han D-W, Kang SH, et al. Cytotoxicity evaluations of pristine graphene and carbon nanotubes in fibroblastic cells. J Korean Phys Soc. 2012;61(6):873-7. https://doi.org/10.3938/jkps.61.873
  35. Shin YC, Lee JH, Kim MJ, Hong SW, Kim B, Hyun JK, et al. Stimulating effect of graphene oxide on myogenesis of C2C12 myoblasts on RGD peptidedecorated PLGA nanofiber matrices. J Biol Eng. 2015;9(1):22. https://doi.org/10.1186/s13036-015-0020-1
  36. Song S-J, Shin YC, Lee HU, Kim B, Han D-W, Lim D. Dose- and timedependent cytotoxicity of layered black phosphorus in fibroblastic cells. Nanomaterials. 2018;8(6):408. https://doi.org/10.3390/nano8060408
  37. Brent JR, Savjani N, Lewis EA, Haigh SJ, Lewis DJ, O'Brien P. Production of few-layer phosphorene by liquid exfoliation of black phosphorus. Chem Commun. 2014;50(87):13338-41. https://doi.org/10.1039/C4CC05752J
  38. Liu H, Neal AT, Zhu Z, Luo Z, Xu X, Tomanek D, et al. Phosphorene: an unexplored 2D semiconductor with a high hole mobility. ACS Nano. 2014;8(4):4033-41. https://doi.org/10.1021/nn501226z
  39. Sun Z, Xie H, Tang S, Yu XF, Guo Z, Shao J, et al. Ultrasmall black phosphorus quantum dots: synthesis and use as photothermal agents. Angew Chem. 2015;127(39):11688-92. https://doi.org/10.1002/ange.201506154
  40. Zhang X, Zhang Z, Zhang S, Li D, Ma W, Ma C, et al. Size effect on the cytotoxicity of layered black phosphorus and underlying mechanisms. Small. 2017;13(32):1701210. https://doi.org/10.1002/smll.201701210
  41. Peng J, Gao W, Gupta BK, Liu Z, Romero-Aburto R, Ge L, et al. Graphene quantum dots derived from carbon fibers. Nano Lett. 2012;12(2):844-9. https://doi.org/10.1021/nl2038979
  42. Shang W, Zhang X, Zhang M, Fan Z, Sun Y, Han M, et al. The uptake mechanism and biocompatibility of graphene quantum dots with human neural stem cells. Nanoscale. 2014;6(11):5799-806. https://doi.org/10.1039/C3NR06433F
  43. Gokhale R, Singh P. Blue luminescent graphene quantum dots by photochemical stitching of small aromatic molecules: fluorescent nanoprobes in cellular imaging. Part Part Syst Charact. 2014;31(4):433-8. https://doi.org/10.1002/ppsc.201300294
  44. Sohaebuddin SK, Thevenot PT, Baker D, Eaton JW, Tang LP. Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol. 2010;7:22. https://doi.org/10.1186/1743-8977-7-22
  45. Akhavan O, Ghaderi E, Akhavan A. Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials. 2012;33(32):8017-25. https://doi.org/10.1016/j.biomaterials.2012.07.040
  46. Kim MJ, Lee JH, Shin YC, Jin L, Hong SW, Han D-W, et al. Stimulated myogenic differentiation of C2C12 murine myoblasts by using graphene oxide. J Korean Phys Soc. 2015;67(11):1910-4. https://doi.org/10.3938/jkps.67.1910
  47. Asati A, Santra S, Kaittanis C, Perez JM. Surface-charge-dependent cell localization and cytotoxicity of cerium oxide nanoparticles. ACS Nano. 2010;4(9):5321-31. https://doi.org/10.1021/nn100816s
  48. Bhattacharjee S, de Haan LHJ, Evers NM, Jiang X, Marcelis ATM, Zuilhof H, et al. Role of surface charge and oxidative stress in cytotoxicity of organic monolayer-coated silicon nanoparticles towards macrophage NR8383 cells. Part Fibre Toxicol. 2010;7(1):25. https://doi.org/10.1186/1743-8977-7-25
  49. Frohlich E. The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomedicine. 2012;7:5577.
  50. Bhattacharjee S, Ershov D, Jvd G, Alink GM, IMCM R, Zuilhof H, et al. Surface charge-specific cytotoxicity and cellular uptake of tri-block copolymer nanoparticles. Nanotoxicology. 2013;7(1):71-84. https://doi.org/10.3109/17435390.2011.633714
  51. Chithrani BD, Ghazani AA, Chan WCW. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 2006;6(4):662-8. https://doi.org/10.1021/nl052396o
  52. Wang S, Lu W, Tovmachenko O, Rai US, Yu H, Ray PC. Challenge in understanding size and shape dependent toxicity of gold nanomaterials in human skin keratinocytes. Chem Phys Lett. 2008;463(1-3):145-9. https://doi.org/10.1016/j.cplett.2008.08.039
  53. Hamilton RF, Wu N, Porter D, Buford M, Wolfarth M, Holian A. Particle length-dependent titanium dioxide nanomaterials toxicity and bioactivity. Part Fibre Toxicol. 2009;6(1):35. https://doi.org/10.1186/1743-8977-6-35
  54. Chen W, Ouyang J, Liu H, Chen M, Zeng K, Sheng J, et al. Black phosphorus nanosheet-based drug delivery system for synergistic photodynamic/photothermal/chemotherapy of cancer. Adv Mater. 2017;29(5):1603864. https://doi.org/10.1002/adma.201603864
  55. Sun X, Liu Z, Welsher K, Robinson JT, Goodwin A, Zaric S, et al. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 2008;1(3):203-12. https://doi.org/10.1007/s12274-008-8021-8
  56. Yang K, Hu L, Ma X, Ye S, Cheng L, Shi X, et al. Multimodal imaging guided photothermal therapy using functionalized graphene nanosheets anchored with magnetic nanoparticles. Adv Mater. 2012;24(14):1868-72. https://doi.org/10.1002/adma.201104964
  57. Nurunnabi MD, Khatun Z, Reeck GR, Lee DY, Lee Y-k. Near infra-red photoluminescent graphene nanoparticles greatly expand their use in noninvasive biomedical imaging. Chem Commun. 2013;49(44):5079-81. https://doi.org/10.1039/c3cc42334d
  58. Cheng L, Liu J, Gu X, Gong H, Shi X, Liu T, et al. PEGylated $WS_{2}$ nanosheets as a multifunctional theranostic agent for in vivo dual-modal CT/photoacoustic imaging guided photothermal therapy. Adv Mater. 2014;26(12):1886-93. https://doi.org/10.1002/adma.201304497
  59. Liu T, Shi S, Liang C, Shen S, Cheng L, Wang C, et al. Iron oxide decorated $MoS_{2}$ nanosheets with double PEGylation for chelator-free radiolabeling and multimodal imaging guided photothermal therapy. ACS Nano. 2015;9(1):950-60. https://doi.org/10.1021/nn506757x
  60. Li Z, Wong SL. Functionalization of 2D transition metal dichalcogenides for biomedical applications. Mater Sci Eng C. 2017;70:1095-106. https://doi.org/10.1016/j.msec.2016.03.039
  61. Duch MC, Budinger GRS, Liang YT, Soberanes S, Urich D, Chiarella SE, et al. Minimizing oxidation and stable nanoscale dispersion improves the biocompatibility of graphene in the lung. Nano Lett. 2011;11(12):5201-7. https://doi.org/10.1021/nl202515a
  62. Zhang X, Yin J, Peng C, Hu W, Zhu Z, Li W, et al. Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration. Carbon. 2011;49(3):986-95. https://doi.org/10.1016/j.carbon.2010.11.005
  63. Jakus AE, Secor EB, Rutz AL, Jordan SW, Hersam MC, Shah RN. Threedimensional printing of high-content graphene scaffolds for electronic and biomedical applications. ACS Nano. 2015;9(4):4636-48. https://doi.org/10.1021/acsnano.5b01179
  64. Hao J, Song G, Liu T, Yi X, Yang K, Cheng L, et al. In vivo long-term biodistribution, excretion, and toxicology of PEGylated transition-metal dichalcogenides $MS_{2}$ (M = Mo, W, Ti) nanosheets. Adv Sci. 2017;4(1):1600160. https://doi.org/10.1002/advs.201600160
  65. Shao J, Xie H, Huang H, Li Z, Sun Z, Xu Y, et al. Biodegradable black phosphorus-based nanospheres for in vivo photothermal cancer therapy. Nat Commun. 2016;7:12967. https://doi.org/10.1038/ncomms12967
  66. Kramer GF, Ames BN. Oxidative mechanisms of toxicity of low-intensity near-UV light in Salmonella typhimurium. J Bacteriol. 1987;169(5):2259-66. https://doi.org/10.1128/jb.169.5.2259-2266.1987
  67. Imlay JA, Linn S. DNA damage and oxygen radical toxicity. Science. 1988;240(4857):1302-9. https://doi.org/10.1126/science.3287616
  68. Stierner U, Rosdahl I, Augustsson A, Kagedal B. UVB irradiation induces melanocyte increase in both exposed and shielded human skin. J Invest Dermatol. 1989;92(4):561-4. https://doi.org/10.1111/1523-1747.ep12709572
  69. Zhuang L, Wang B, Sauder DN. Molecular mechanism of ultraviolet-induced keratinocyte apoptosis. J Interf Cytokine Res. 2000;20(5):445-54. https://doi.org/10.1089/10799900050023852

Cited by

  1. Comparison of cytotoxicity of black phosphorus nanosheets in different types of fibroblasts vol.23, pp.1, 2018, https://doi.org/10.1186/s40824-019-0174-x
  2. Property-Activity Relationship of Black Phosphorus at the Nano-Bio Interface: From Molecules to Organisms vol.120, pp.4, 2018, https://doi.org/10.1021/acs.chemrev.9b00445
  3. Black phosphorus as a versatile nanoplatform: From unique properties to biomedical applications vol.13, pp.5, 2018, https://doi.org/10.1142/s1793545820300086
  4. MXene and black phosphorus based 2D nanomaterials in bioimaging and biosensing: progress and perspectives vol.9, pp.26, 2018, https://doi.org/10.1039/d1tb00410g
  5. Spontaneously promoted osteogenic differentiation of MC3T3-E1 preosteoblasts on ultrathin layers of black phosphorus vol.128, pp.None, 2018, https://doi.org/10.1016/j.msec.2021.112309
  6. Antipathogenic properties and applications of low-dimensional materials vol.12, pp.1, 2021, https://doi.org/10.1038/s41467-021-23278-7
  7. Bioengineering applications of black phosphorus and their toxicity assessment vol.8, pp.12, 2018, https://doi.org/10.1039/d1en00273b
  8. Memory effects in black phosphorus field effect transistors vol.9, pp.1, 2022, https://doi.org/10.1088/2053-1583/ac3f45