Carbon Nanomaterials for Optical Bioimaging and Phototherapy
Haifeng Dong
Beijing Key Laboratory for Bioengineering and Sensing Technology, Research Center for Bioengineering and Sensing Technology, School of Chemistry & Biological Engineering, University of Science & Technology, Beijing, PR China
Search for more papers by this authorYu Cao
Beijing Key Laboratory for Bioengineering and Sensing Technology, Research Center for Bioengineering and Sensing Technology, School of Chemistry & Biological Engineering, University of Science & Technology, Beijing, PR China
Search for more papers by this authorHaifeng Dong
Beijing Key Laboratory for Bioengineering and Sensing Technology, Research Center for Bioengineering and Sensing Technology, School of Chemistry & Biological Engineering, University of Science & Technology, Beijing, PR China
Search for more papers by this authorYu Cao
Beijing Key Laboratory for Bioengineering and Sensing Technology, Research Center for Bioengineering and Sensing Technology, School of Chemistry & Biological Engineering, University of Science & Technology, Beijing, PR China
Search for more papers by this authorYuen Yung Hui
Institute of Atomic and Molecular Sciences, Academia Sinica, Taipei, Republic of China
Search for more papers by this authorHuan-Cheng Chang
Institute of Atomic and Molecular Sciences, Academia Sinica, Taipei, Republic of China
Search for more papers by this authorHaifeng Dong
University of Science and Technology Beijing, P.R. China
Search for more papers by this authorXueji Zhang
University of Science and Technology Beijing, P.R. China
Search for more papers by this authorSummary
This chapter covers the recent progress in optical biological imaging analysis and phototherapies using carbon nanomaterials. Different carbon nanomaterials require different strategies of surface functionalization to make them soluble in aqueous environment and compatible with cells and tissues. Several spectroscopic techniques can be utilized for biological in vitro and in vivo imaging. One of the most common techniques is fluorescence imaging. Carbon nanomaterials can be used for their intrinsic fluorescence properties or can be tagged with fluorescent molecules. Phototherapies, mainly including photothermal therapy (PTT) and photodynamic therapy (PDT), are able to destruct cancer cells upon specific light irradiation. With the help of nanotechnology, phototherapeutic nanoagents could specifically target cancer via either passive or active tumor targeting. In the past few years, phototherapies based on the unique optical and chemical properties of carbon nanomaterials have aroused increasing interest.
References
- Siegel, R.L., Miller, K.D., and Jemal, A. (2016). Cancer statistics, 2016. CA Cancer J. Clin. 66 (1): 7–30.
- Chen, D., Dougherty, C.A., Zhu, K. et al. (2015). Theranostic applications of carbon nanomaterials in cancer: focus on imaging and cargo delivery. J. Controlled Release 210: 230–245.
- Koo, H., Huh, M.S., Ryu, J.H. et al. (2011). Nanoprobes for biomedical imaging in living systems. Nano Today 6 (2): 204–220.
-
Wen, J., Xu, Y., Li, H.
et al. (2015). Recent applications of carbon nanomaterials in fluorescence biosensing and bioimaging. Chem. Commun. (Cambridge)
51 (57): 11346–11358.
10.1039/C5CC02887F Google Scholar
- Etrych, T., Lucas, H., Janouskova, O. et al. (2016). Fluorescence optical imaging in anticancer drug delivery. J. Controlled Release 226: 168–181.
- Parveen, S., Misra, R., and Sahoo, S.K. (2012). Nanoparticles: a boon to drug delivery, therapeutics, diagnostics and imaging. Nanomedicine 8 (2): 147–166.
- Ma, X., Zhao, Y., and Liang, X.J. (2011). Theranostic nanoparticles engineered for clinic and pharmaceutics. Acc. Chem. Res. 44 (10): 1114–1122.
-
Ranjan, S., Jayakumar, M.K., and Zhang, Y. (2015). Luminescent lanthanide nanomaterials: an emerging tool for theranostic applications. Nanomedicine (London)
10 (9): 1477–1491.
10.2217/nnm.14.229 Google Scholar
- Jeong, E.H., Jung, G., Hong, C.A. et al. (2014). Gold nanoparticle (AuNP)-based drug delivery and molecular imaging for biomedical applications. Arch. Pharmacal Res. 37 (1): 53–59.
- Bosi, S., Da Ros, T., Spalluto, G. et al. (2003). Fullerene derivatives: an attractive tool for biological applications. Eur. J. Med. Chem. 38 (11–12): 913–923.
- Waddington, D.E.J., Sarracanie, M., Zhang, H. et al. (2017). Nanodiamond-enhanced MRI via in situ hyperpolarization. Nat. Commun. 8: 15118.
-
Vaijayanthimala, V., Lee, D.K., Kim, S.V.
et al. (2015). Nanodiamond-mediated drug delivery and imaging: challenges and opportunities. Expert Opin. Drug Deliv.
12 (5): 735–749.
10.1517/17425247.2015.992412 Google Scholar
- Bianco, A., Kostarelos, K., and Prato, M. (2005). Applications of carbon nanotubes in drug delivery. Curr. Opin. Chem. Biol. 9 (6): 674–679.
- Ji, S.R., Liu, C., Zhang, B. et al. (2010). Carbon nanotubes in cancer diagnosis and therapy. Biochim. Biophys. Acta 1806 (1): 29–35.
- Yang, G., Zhu, C., Du, D. et al. (2015). Graphene-like two-dimensional layered nanomaterials: applications in biosensors and nanomedicine. Nanoscale 7 (34): 14217–14231.
- Yang, K., Feng, L., Shi, X. et al. (2013). Nano-graphene in biomedicine: theranostic applications. Chem. Soc. Rev. 42 (2): 530–547.
- Lim, S.Y., Shen, W., and Gao, Z. (2015). Carbon quantum dots and their applications. Chem. Soc. Rev. 44 (1): 362–381.
- Hong, G., Diao, S., Antaris, A.L. et al. (2015). Carbon nanomaterials for biological imaging and nanomedicinal therapy. Chem. Rev. 115 (19): 10816–10906.
- Yang, W., Ratinac, K.R., Ringer, S.P. et al. (2010). Carbon nanomaterials in biosensors: should you use nanotubes or graphene? Angew. Chem. Int. Ed. 49 (12): 2114–2138.
- Bai, H., Li, C., and Shi, G. (2011). Functional composite materials based on chemically converted graphene. Adv. Mater. 23 (9): 1089–1115.
-
Hirsch, A. (2002). Functionalization of single-walled carbon nanotubes. Angew. Chem. Int. Ed.
41 (11): 1853.
10.1002/1521-3773(20020603)41:11<1853::AID-ANIE1853>3.0.CO;2-N CAS PubMed Web of Science® Google Scholar
- Lai, L. and Barnard, A.S. (2015). Functionalized nanodiamonds for biological and medical applications. J. Nanosci. Nanotechnol. 15 (2): 989–999.
- Shim, M., Shi Kam, N.W., Chen, R.J. et al. (2002). Functionalization of carbon nanotubes for biocompatibility and biomolecular recognition. Nano Lett. 2 (4): 285–288.
- Prencipe, G., Tabakman, S.M., Welsher, K. et al. (2009). PEG branched polymer for functionalization of nanomaterials with ultralong blood circulation. J. Am. Chem. Soc. 131 (13): 4783–4787.
- Chen, R.J., Bangsaruntip, S., Drouvalakis, K.A. et al. (2003). Noncovalent functionalization of carbon nanotubes for highly specific electronic biosensors. Proc. Natl. Acad. Sci. U. S. A. 100 (9): 4984–4989.
-
Langa, F., de la Cruz, P., Espíldora, E.
et al. (2000). Fullerene chemistry under microwave irradiation. Carbon
38 (11–12): 1641–1646.
10.1016/S0008-6223(99)00284-5 Google Scholar
- Tasis, D., Tagmatarchis, N., Bianco, A. et al. (2006). Chemistry of carbon nanotubes. Chem. Rev. 106 (3): 1105–1136.
- Zhu, S., Zhang, J., Tang, S. et al. (2012). Surface chemistry routes to modulate the photoluminescence of graphene quantum dots: from fluorescence mechanism to up-conversion bioimaging applications. Adv. Funct. Mater. 22 (22): 4732–4740.
- Wang, Y., Li, Z., Wang, J. et al. (2011). Graphene and graphene oxide: biofunctionalization and applications in biotechnology. Trends Biotechnol. 29 (5): 205–212.
- Weissleder, R. (2001). A clearer vision for in vivo imaging. Nat. Biotechnol. 19 (4): 316–317.
- Smith, A.M., Mancini, M.C., and Nie, S. (2009). Bioimaging: second window for in vivo imaging. Nat. Nanotechnol. 4 (11): 710–711.
-
Reuther, U. and Hirsch, A. (2000). Synthesis, properties and chemistry of Aza[60]fullerene. Carbon
38 (11–12): 1539–1549.
10.1016/S0008-6223(00)00053-1 Google Scholar
-
Capozzi, V., Casamassima, G., Lorusso, G.F.
et al. (1996). Optical spectra and photoluminescence of C60 thin films. Solid State Commun.
98 (9): 853–858.
10.1016/0038-1098(96)00060-9 Google Scholar
- Cherukuri, P., Bachilo, S.M., Litovsky, S.H. et al. (2004). Near-infrared fluorescence microscopy of single-walled carbon nanotubes in phagocytic cells. J. Am. Chem. Soc. 126 (48): 15638–15639.
- Heller, D.A., Baik, S.T., Eurell, E. et al. (2005). Single-walled carbon nanotube spectroscopy in live cells: towards long-term labels and optical sensors. Adv. Mater. 17 (23): 2793–2799.
- Carlson, L.J., Maccagnano, S.E., Zheng, M. et al. (2007). Fluorescence efficiency of individual carbon nanotubes. Nano Lett. 7 (12): 3698–3703.
- Crochet, J., Clemens, M., and Hertel, T. (2007). Quantum yield heterogeneities of aqueous single-wall carbon nanotube suspensions. J. Am. Chem. Soc. 129 (26): 8058–8059.
- Lefebvre, J., Austing, D.G., Bond, J. et al. (2006). Photoluminescence imaging of suspended single-walled carbon nanotubes. Nano Lett. 6 (8): 1603–1608.
- Lacerda, L., Pastorin, G., Wu, W. et al. (2006). Luminescence of functionalized carbon nanotubes as a tool to monitor bundle formation and dissociation in water: the effect of plasmid-DNA complexation. Adv. Funct. Mater. 16 (14): 1839–1846.
- Zhu, S., Song, Y., Wang, J. et al. (2017). Photoluminescence mechanism in graphene quantum dots: quantum confinement effect and surface/edge state. Nano Today 13: 10–14.
-
Dekaliuk, M.O., Viagin, O., Malyukin, Y.V.
et al. (2014). Fluorescent carbon nanomaterials: “quantum dots” or nanoclusters?
Phys. Chem. Chem. Phys.
16 (30): 16075–16084.
10.1039/C4CP00138A Google Scholar
- Cao, L., Meziani, M.J., Sahu, S. et al. (2013). Photoluminescence properties of graphene versus other carbon nanomaterials. Acc. Chem. Res. 46 (1): 171–180.
- Havlik, J., Petrakova, V., Rehor, I. et al. (2013). Boosting nanodiamond fluorescence: towards development of brighter probes. Nanoscale 5 (8): 3208–3211.
- Mochalin, V.N., Shenderova, O., Ho, D. et al. (2011). The properties and applications of nanodiamonds. Nat. Nanotechnol. 7 (1): 11–23.
- Levi, N., Hantgan, R.R., Lively, M.O. et al. (2006). C60-fullerenes: detection of intracellular photoluminescence and lack of cytotoxic effects. J. Nanobiotechnol. 4: 14.
- Jeong, J., Jung, J., Choi, M. et al. (2012). Color-tunable photoluminescent fullerene nanoparticles. Adv. Mater. 24 (15): 1999–2003.
- Kwag, D.S., Park, K., Oh, T. et al. (2013). Hyaluronated fullerenes with photoluminescent and antitumoral activity. Chem. Commun. (Cambridge) 49 (3): 282–284.
- Zheng, X.T., Ananthanarayanan, A., Luo, K.Q. et al. (2015). Glowing graphene quantum dots and carbon dots: properties, syntheses, and biological applications. Small 11 (14): 1620–1636.
- Hola, K., Zhang, Y., Wang, Y. et al. (2014). Carbon dots—emerging light emitters for bioimaging, cancer therapy and optoelectronics. Nano Today 9 (5): 590–603.
- Zhu, S., Zhang, J., Qiao, C. et al. (2011). Strongly green-photoluminescent graphene quantum dots for bioimaging applications. Chem. Commun. (Cambridge) 47 (24): 6858–6860.
- Cao, L., Wang, X., Meziani, M.J. et al. (2007). Carbon dots for multiphoton bioimaging. J. Am. Chem. Soc. 129 (37): 11318–11319.
- Liu, H., Na, W., Liu, Z. et al. (2017). A novel turn-on fluorescent strategy for sensing ascorbic acid using graphene quantum dots as fluorescent probe. Biosens. Bioelectron. 92: 229–233.
- Fan, Z., Zhou, S., Garcia, C. et al. (2017). pH-responsive fluorescent graphene quantum dots for fluorescence-guided cancer surgery and diagnosis. Nanoscale 9 (15): 4928–4933.
- Sun, H., Wu, L., Gao, N. et al. (2013). Improvement of photoluminescence of graphene quantum dots with a biocompatible photochemical reduction pathway and its bioimaging application. ACS Appl. Mater. Interfaces 5 (3): 1174–1179.
- Lu, S., Sui, L., Liu, J. et al. (2017). Near-infrared photoluminescent polymer-carbon nanodots with two-photon fluorescence. Adv. Mater. 29 (15).
- Liu, Q., Guo, B., Rao, Z. et al. (2013). Strong two-photon-induced fluorescence from photostable, biocompatible nitrogen-doped graphene quantum dots for cellular and deep-tissue imaging. Nano Lett. 13 (6): 2436–2441.
-
Neves, V., Gerondopoulos, A., Heister, E.
et al. (2012). Cellular localization, accumulation and trafficking of double-walled carbon nanotubes in human prostate cancer cells. Nano Res.
5 (4): 223–234.
10.1007/s12274-012-0202-9 Google Scholar
- Leeuw, T.K., Reith, R.M., Simonette, R.A. et al. (2007). Single-walled carbon nanotubes in the intact organism: near-IR imaging and biocompatibility studies in Drosophila . Nano Lett. 7 (9): 2650–2654.
- Welsher, K., Liu, Z., Sherlock, S.P. et al. (2009). A route to brightly fluorescent carbon nanotubes for near-infrared imaging in mice. Nat. Nanotechnol. 4 (11): 773–780.
- Sun, X., Liu, Z., Welsher, K. et al. (2008). Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 1 (3): 203–212.
- Fu, C.C., Lee, H.Y., Chen, K. et al. (2007). Characterization and application of single fluorescent nanodiamonds as cellular biomarkers. Proc. Natl. Acad. Sci. U. S. A. 104 (3): 727–732.
- Yu, S.J., Kang, M.W., Chang, H.C. et al. (2005). Bright fluorescent nanodiamonds: no photobleaching and low cytotoxicity. J. Am. Chem. Soc. 127 (50): 17604–17605.
- Faklaris, O., Joshi, V., Irinopoulou, T. et al. (2009). Photoluminescent diamond nanoparticles for cell labeling: study of the uptake mechanism in mammalian cells. ACS Nano 3 (12): 3955–3962.
- Mohan, N., Chen, C.S., Hsieh, H.H. et al. (2010). In vivo imaging and toxicity assessments of fluorescent nanodiamonds in Caenorhabditis elegans . Nano Lett. 10 (9): 3692–3699.
- Mohan, N., Zhang, B., Chang, C.-C. et al. (2011). Fluorescent nanodiamond – a novel nanomaterial for in vivo applications. MRS Proc. 1362.
- Vaijayanthimala, V., Cheng, P.Y., Yeh, S.H. et al. (2012). The long-term stability and biocompatibility of fluorescent nanodiamond as an in vivo contrast agent. Biomaterials 33 (31): 7794–7802.
- Pantarotto, D., Briand, J.P., Prato, M. et al. (2004). Translocation of bioactive peptides across cell membranes by carbon nanotubes. Chem. Commun. (Cambridge) (1): 16–17.
- Nakayama-Ratchford, N., Bangsaruntip, S., Sun, X. et al. (2007). Noncovalent functionalization of carbon nanotubes by fluorescein-polyethylene glycol: supramolecular conjugates with pH-dependent absorbance and fluorescence. J. Am. Chem. Soc. 129 (9): 2448–2449.
- Kam, N.W., Liu, Z., and Dai, H. (2006). Carbon nanotubes as intracellular transporters for proteins and DNA: an investigation of the uptake mechanism and pathway. Angew. Chem. Int. Ed. 45 (4): 577–581.
- Yang, K., Zhang, S., Zhang, G. et al. (2010). Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett. 10 (9): 3318–3323.
- Yang, K., Wan, J., Zhang, S. et al. (2011). In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano 5 (1): 516–522.
- Hong, H., Yang, K., Zhang, Y. et al. (2012). In vivo targeting and imaging of tumor vasculature with radiolabeled, antibody-conjugated nanographene. ACS Nano 6 (3): 2361–2370.
- Chang, I.P., Hwang, K.C., and Chiang, C.S. (2008). Preparation of fluorescent magnetic nanodiamonds and cellular imaging. J. Am. Chem. Soc. 130 (46): 15476–15481.
- Zhang, X.Q., Lam, R., Xu, X. et al. (2011). Multimodal nanodiamond drug delivery carriers for selective targeting, imaging, and enhanced chemotherapeutic efficacy. Adv. Mater. 23 (41): 4770–4775.
- Salaam, A.D., Hwang, P., McIntosh, R. et al. (2014). Nanodiamond-DGEA peptide conjugates for enhanced delivery of doxorubicin to prostate cancer. Beilstein J. Nanotechnol. 5: 937–945.
- Rai, P., Mallidi, S., Zheng, X. et al. (2010). Development and applications of photo-triggered theranostic agents. Adv. Drug Delivery Rev. 62 (11): 1094–1124.
- Menon, J.U., Jadeja, P., Tambe, P. et al. (2013). Nanomaterials for photo-based diagnostic and therapeutic applications. Theranostics 3 (3): 152–166.
- Shen, Y., Shuhendler, A.J., Ye, D. et al. (2016). Two-photon excitation nanoparticles for photodynamic therapy. Chem. Soc. Rev. 45 (24): 6725–6741.
- Chakrabarti, M., Kiseleva, R., Vertegel, A. et al. (2015). Carbon nanomaterials for drug delivery and cancer therapy. J. Nanosci. Nanotechnol. 15 (8): 5501–5511.
- Liu, Z., Chen, K., Davis, C. et al. (2008). Drug delivery with carbon nanotubes for in vivo cancer treatment. Cancer Res. 68 (16): 6652–6660.
- Zou, L., Wang, H., He, B. et al. (2016). Current approaches of photothermal therapy in treating cancer metastasis with nanotherapeutics. Theranostics 6 (6): 762–772.
- Chen, Q., Wen, J., Li, H. et al. (2016). Recent advances in different modal imaging-guided photothermal therapy. Biomaterials 106: 144–166.
-
Chen, Y., Wang, L., and Shi, J. (2016). Two-dimensional non-carbonaceous materials-enabled efficient photothermal cancer therapy. Nano Today
11 (3): 292–308.
10.1016/j.nantod.2016.05.009 Google Scholar
- Zheng, T., Li, G.G., Zhou, F. et al. (2016). Gold-nanosponge-based multistimuli-responsive drug vehicles for targeted chemo-photothermal therapy. Adv. Mater. 28 (37): 8218–8226.
- Lee, C., Hwang, H.S., Lee, S. et al. (2017). Rabies virus-inspired silica-coated gold nanorods as a photothermal therapeutic platform for treating brain tumors. Adv. Mater. 29 (13): 1605563.
- Chen, W., Zhang, S., Yu, Y. et al. (2016). Structural-engineering rationales of gold nanoparticles for cancer theranostics. Adv. Mater. 28 (39): 8567–8585.
- Ji, M., Xu, M., Zhang, W. et al. (2016). Structurally well-defined Au@Cu2 − xS core-shell nanocrystals for improved cancer treatment based on enhanced photothermal efficiency. Adv. Mater. 28 (16): 3094–3101.
- Wang, Z., Huang, P., Jacobson, O. et al. (2016). Biomineralization-inspired synthesis of copper sulfide-ferritin nanocages as cancer theranostics. ACS Nano 10 (3): 3453–3460.
-
Riedinger, A., Avellini, T., Curcio, A.
et al. (2015). Post-synthesis incorporation of 64Cu in CuS nanocrystals to radiolabel photothermal probes: a feasible approach for clinics. J. Am. Chem. Soc.
137 (48): 15145–15151.
10.1021/jacs.5b07973 Google Scholar
- Lyu, Y., Xie, C., Chechetka, S.A. et al. (2016). Semiconducting polymer nanobioconjugates for targeted photothermal activation of neurons. J. Am. Chem. Soc. 138 (29): 9049–9052.
- Moon, H.K., Lee, S.H., and Choi, H.C. (2009). In vivo near-infrared mediated tumor destruction by photothermal effect of carbon nanotubes. ACS Nano 3 (11): 3707–3713.
- Robinson, J.T., Welsher, K., Tabakman, S.M. et al. (2010). High performance in vivo near-IR (>1 mum) imaging and photothermal cancer therapy with carbon nanotubes. Nano Res. 3 (11): 779–793.
-
Wang, D., Hou, C., Meng, L.
et al. (2017). Stepwise growth of gold coated cancer targeting carbon nanotubes for the precise delivery of doxorubicin combined with photothermal therapy. J. Mater. Chem. B
5 (7): 1380–1387.
10.1039/C6TB02755E Google Scholar
- Wang, S., Lin, Q., Chen, J. et al. (2017). Biocompatible polydopamine-encapsulated gadolinium-loaded carbon nanotubes for MRI and color mapping guided photothermal dissection of tumor metastasis. Carbon 112: 53–62.
- Balandin, A.A. (2011). Thermal properties of graphene and nanostructured carbon materials. Nat. Mater. 10 (8): 569–581.
- Robinson, J.T., Tabakman, S.M., Liang, Y. et al. (2011). Ultrasmall reduced graphene oxide with high near-infrared absorbance for photothermal therapy. J. Am. Chem. Soc. 133 (17): 6825–6831.
- Castano, A.P., Mroz, P., and Hamblin, M.R. (2006). Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 6 (7): 535–545.
- Celli, J.P., Spring, B.Q., Rizvi, I. et al. (2010). Imaging and photodynamic therapy: mechanisms, monitoring, and optimization. Chem. Rev. 110 (5): 2795–2838.
- Detty, M.R., Gibson, S.L., and Wagner, S.J. (2004). Current clinical and preclinical photosensitizers for use in photodynamic therapy. J. Med. Chem. 47 (16): 3897–3915.
- Markovic, Z. and Trajkovic, V. (2008). Biomedical potential of the reactive oxygen species generation and quenching by fullerenes (C60). Biomaterials 29 (26): 3561–3573.
- Mroz, P., Xia, Y., Asanuma, D. et al. (2011). Intraperitoneal photodynamic therapy mediated by a fullerene in a mouse model of abdominal dissemination of colon adenocarcinoma. Nanomedicine 7 (6): 965–974.
- Shi, J., Yu, X., Wang, L. et al. (2013). PEGylated fullerene/iron oxide nanocomposites for photodynamic therapy, targeted drug delivery and MR imaging. Biomaterials 34 (37): 9666–9677.
- Murakami, T., Nakatsuji, H., Inada, M. et al. (2012). Photodynamic and photothermal effects of semiconducting and metallic-enriched single-walled carbon nanotubes. J. Am. Chem. Soc. 134 (43): 17862–17865.
-
Wang, L., Shi, J., Liu, R.
et al. (2014). Photodynamic effect of functionalized single-walled carbon nanotubes: a potential sensitizer for photodynamic therapy. Nanoscale
6 (9): 4642–4651.
10.1039/C3NR06835H Google Scholar
-
Lee, D.J., Park, S.Y., Oh, Y.T.
et al. (2011). Preparation of chlorine e6-conjugated single-wall carbon nanotube for photodynamic therapy. Macromol. Res.
19 (8): 848–852.
10.1007/s13233-011-0816-x Google Scholar
- Tian, B., Wang, C., Zhang, S. et al. (2011). Photothermally enhanced photodynamic therapy delivered by nano-graphene oxide. ACS Nano 5 (9): 7000–7009.
- Huang, P., Xu, C., Lin, J. et al. (2011). Folic acid-conjugated graphene oxide loaded with photosensitizers for targeting photodynamic therapy. Theranostics 1: 240–250.
- Markovic, Z.M., Ristic, B.Z., Arsikin, K.M. et al. (2012). Graphene quantum dots as autophagy-inducing photodynamic agents. Biomaterials 33 (29): 7084–7092.
- Ristic, B.Z., Milenkovic, M.M., Dakic, I.R. et al. (2014). Photodynamic antibacterial effect of graphene quantum dots. Biomaterials 35 (15): 4428–4435.
- Ge, J., Lan, M., Zhou, B. et al. (2014). A graphene quantum dot photodynamic therapy agent with high singlet oxygen generation. Nat. Commun. 5: 4596.