Aptamer-based selective KB cell killing by the photothermal effect of gold nanorods

Abstract

Development of both specific receptors against target cancer cells and therapeutic tools using receptor-functionalized nanoplatforms are important in cancer treatment. To address these challenges, we developed KB cell–specific aptamers using systematic evolution of ligands by exponential enrichment (SELEX). Additionally, we combined the targeting properties of aptamers and photothermal characteristics of GNRs. As a result, we generated efficient aptamer-gold nanorods (Apt-GNRs) targeting KB cancer cells and exhibiting photothermal therapeutic effects. When the samples were irradiated with a light-emitting diode at 845 nm, the targeted KB cells showed ~ 80% cell death compared with the unirradiated and aptamer-free control. Based on the low toxicity, biocompatibility, and selectivity of Apt-GNRs, the proposed nanoplatform has significant potential as a cancer therapy in vivo.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Alkilany AM, Thompson LB, Boulos SP, Sisco PN, Murphy CJ (2012) Gold nanorods: their potential for photothermal therapeutics and drug delivery, tempered by the complexity of their biological interactions. Adv Drug Deliv Rev 64:190–199

    CAS  Article  Google Scholar 

  2. Black KCL, Yi J, Rivera JG, Zelasko-Leon DC, Messersmithc PB (2013) Biomimetic polydopamine coating on gold nanorods for biofunctionalization, imaging, and photothermal therapy. Proc of SPIE 8598(2013):85980D

    Article  Google Scholar 

  3. Burrows ND, Lin W, Hinman JG, Dennison JM, Vartanian AM, Abadeer NS, Grzincic EM, Jacob LM, Li J, Murphy CJ (2016) Surface chemistry of gold nanorods. Langmuir 32:9905–9921

    CAS  Article  Google Scholar 

  4. Cao F, Yao Q, Yang T, Zhang Z, Han Y, Feng J, Wang X (2016) Marriage of antibody–drug conjugate with gold nanorods to achieve multi-modal ablation of breast cancer cells and enhanced photoacoustic performance. RSC Adv 6:46594–46606

    CAS  Article  Google Scholar 

  5. Chandrasekaran R, Lee AS, Yap LW, Jans DA, Wagstaff KM, Cheng W (2016) Tumor cell-specific photothermal killing by SELEX-derived DNA aptamer-targeted gold nanorods. Nanoscale 8:187–196

    CAS  Article  Google Scholar 

  6. Charan S, Sanjiv K, Singh N, Chien FC, Chen YF, Nergui NN, Huang SH, Kuo CW, Lee TC, Chen P (2012) Development of chitosan oligosaccharide-modified gold nanorods for in vivo targeted delivery and noninvasive imaging by NIR irradiation. Bioconjug Chem 23:2173–2182

    CAS  Article  Google Scholar 

  7. Choi J, Park Y, Choi EB, Kim HO, Kim DJ, Hong Y, Ryu SH, Lee JH, Suh JS, Yang J, Huh YM, Haam S (2014) Aptamer-conjugated gold nanorod for photothermal ablation of epidermal growth factor receptor-overexpressed epithelial cancer. J Biomed Opt 19:051203

    Article  Google Scholar 

  8. Fekrazad R, Afzali M, Pasban-Aliabadi H, Esmaeili-Mahani S, Aminizadeh M, Mostafavi A (2017) Cytotoxic effect of thymus caramanicus jalas on human oral epidermoid carcinoma KB cells. Braz Dent J 28:72–77

    Article  Google Scholar 

  9. Gallina ME, Zhou Y, Johnson CJ, Harris-Birtill D, Singh M, Zhao H, Ma D, Cass T, Elson DS (2016) Aptamer-conjugated, fluorescent gold nanorods as potential cancer theradiagnostic agents. Mater Sci Eng C Mater Biol Appl 59:324–332

    CAS  Article  Google Scholar 

  10. Huang YF, Sefah K, Bamrungsap S, Chang HT, Tan W (2008) Selective photothermal therapy for mixed cancer cells using aptamer-conjugated nanorods. Langmuir 24:11860–11865

    CAS  Article  Google Scholar 

  11. Kim H, Chang JH (2014) Dual thermal therapeutic method for selective treatment of deep-lying tissue. IEEE Int Ultrason Symp 6932195:21–24

    Google Scholar 

  12. Kim JS, Oh D, Yim MJ, Park JJ, Kang KR, Cho IA, Moon SM, Oh JS, You JS, Kim CS, Kim DK, Lee SY, Lee GJ, Im HJ, Kim SG (2015) Berberine induces FasL-related apoptosis through p38 activation in KB human oral cancer cells. Oncol Rep 33:1775–1782

    CAS  Article  Google Scholar 

  13. Li J, Zhu B, Zhu Z, Zhang Y, Yao X, Tu S, Liu R, Jia S, Yang CJ (2015) Simple and rapid functionalization of gold nanorods with oligonucleotides using a mPEG-SH/tween 20-assisted approach. Langmuir 31:7869–7876

    CAS  Article  Google Scholar 

  14. Li Y, Zhang Y, Zhao M, Zhou Q, Wang L, Wang H, Wang X, Zhan L (2016) A simple aptamer- functionalized gold nanorods based biosensor for the sensitive detection of MCF-7 breast cancer cells. Chem Commun 52:3959–3961

    CAS  Article  Google Scholar 

  15. Li TK, Yin K, Chen Z, Bao Y, Zhang SX (2017) MiR-214 regulates oral cancer KB cell apoptosis through targeting RASSF5. Genet Mol Res 16:gmr16019327

    Google Scholar 

  16. Ma Z, Xia H, Liu Y, Liu B, Chen W, Zhao Y (2013) Applications of gold nanorods in biomedical imaging and related fields. Chin Sci Bull 58:2530–2536

    CAS  Article  Google Scholar 

  17. Manivasagan P, Hoang G, Santha Moorthy M, Mondal S, Minh Doan VH, Kim H, Vy Phan TT, Nguyen TP, Oh J (2019) Chitosan/fucoidan multilayer coating of gold nanorods as highly efficient near-infrared photothermal agents for cancer therapy. Carbohydr Polym 211:360–369

    CAS  Article  Google Scholar 

  18. Neshastehriz A, Tabei M, Maleki S, Eynali S, Shakeri-Zadeh A (2017) Photothermal therapy using folate conjugated gold nanoparticles enhances the effects of 6 MV X-ray on mouth epidermal carcinoma cells. J Photochem Photobiol B 172:52–60

    CAS  Article  Google Scholar 

  19. Nguyen KT (2012) Photothermal therapy and nanomaterials. J Bioeng Biomed Sci 2:1000e112

    Article  Google Scholar 

  20. Oh MH, Yu JH, Kim I, Nam YS (2015) Genetically programmed clusters of gold nanoparticles for cancer cell-targeted photothermal therapy. ACS Appl Mater Interfaces 7:22578–22586

    CAS  Article  Google Scholar 

  21. Pang X, Cui C, Wan S, Jiang Y, Zhang L, Xia L, Li L, Li X, Tan W (2018) Bioapplications of cell-SELEX-generated aptamers in cancer diagnostics. Ther Theranostics and Biomarker Discov: A Comprehensive Review Cancers 10:E47

    Google Scholar 

  22. Qin J, Peng Z, Li B, Ye K, Zhang Y, Yuan F, Yang X, Huang L, Hu J, Lu X (2015) Gold nanorods as a theranostic platform for in vitro and in vivo imaging and photothermal therapy of inflammatory macrophages. Nanoscale 7:13991–14001

    CAS  Article  Google Scholar 

  23. Raji V, Kumar J, Rejiya CS, Vibin M, Shenoi VN, Abraham A (2011) Selective photothermal efficiency of citrate capped gold nanoparticles for destruction of cancer cells. Exp Cell Res 317:2052–2058

    CAS  Article  Google Scholar 

  24. Ruff J, Steitz J, Buchkremer A, Noyong M, Hartmann H, Besmehnc A, Simon U (2016) Multivalency of PEG-thiol ligands affects the stability of NIR-absorbing hollow gold nanospheres and gold nanorods. J Mater Chem B 4:2828–2841

    CAS  Article  Google Scholar 

  25. Samim M, Prashant CK, Dinda AK, Maitra AN, Arora I (2011) Synthesis and characterization of gold nanorods and their application for photothermal cell damage. Int J Nanomedicine 6:1825–1831

    Article  Google Scholar 

  26. Scully C (2011) Oral cancer aetiopathogenesis; past, present and future aspects. Med Oral Patol Oral Cir Bucal 3:e306–e311

    Article  Google Scholar 

  27. Shokri R, Salouti M, Zanjani RS (2015) Anti protein an antibody-gold nanorods conjugate: a targeting agent for selective killing of methicillin resistant staphylococcus aureus using photothermal therapy method. J Microbiol 53:116–121

    CAS  Article  Google Scholar 

  28. Siegel RL, Miller KD, Jemal A (2017) Cancer statistics, 2017. CA Cancer J Clin 67:7–30

    Article  Google Scholar 

  29. Skouridou V, Jauset-Rubio M, Ballester P, Bashammakh AS, El-Shahawi MS, Alyoubi AO, O’Sullivan CK (2017) Selection and characterization of DNA aptamers against the steroid testosterone. Microchim Acta 184:1631–1639

    CAS  Article  Google Scholar 

  30. Sugerman PB, Savage NW (1999) Current concepts in oral cancer. Aust Dent J 44:147–156

    CAS  Article  Google Scholar 

  31. Wang J, Zhu G, You M, Song E, Shukoor MI, Zhang K, Altman MB, Chen Y, Zhu Z, Huang CZ, Tan W (2012) Assembly of aptamer switch probes and photosensitizer on gold nanorods for targeted photothermal and photodynamic cancer therapy. ACS Nano 6:5070–5077

    CAS  Article  Google Scholar 

  32. Wang J, You M, Zhu G, Shukoor MI, Chen Z, Zhao Z, Altman MB, Yuan Q, Zhu Z, Chen Y, Huang CZ, Tan W (2013) Photosensitizer-gold nanorod composite for targeted multimodal therapy. Small 9:3678–3684

    CAS  Article  Google Scholar 

  33. Wang X, Gao W, Fan H, Ding D, Lai X, Zou Y, Chen L, Chen Z, Tan W (2016) Simultaneous tracking of drug molecules and carriers using aptamer-functionalized fluorescent superstable gold nanorod-carbon nanocapsules during thermo-chemotherapy. Nanoscale 8:7942–7948

    CAS  Article  Google Scholar 

  34. Wang L, Wang R, Chen F, Jiang T, Wang H, Slavik M, Wei H, Li Y (2017a) QCM-based aptamer selection and detection of Salmonella typhimurium. Food Chem 221:776–782

    CAS  Article  Google Scholar 

  35. Wang H, Wang J, Wang Q, Chen X, Liu M, Chen H, Pei R (2017b) Selection and characterization of dimethylindole red DNA aptamers for the development of light-up fluorescent probes. Talanta 168:217–221

    CAS  Article  Google Scholar 

  36. World Health Organization (2018) Fact sheet on cancer. WHO, Geneva, Switzerland

    Google Scholar 

  37. Yang Y, Liu J, Sun X, Feng L, Zhu W, Liu Z, Chen M (2016) Near-infrared light-activated cancer cell targeting and drug delivery with aptamer-modified nanostructures. Nano Res 9:139–148

    CAS  Article  Google Scholar 

  38. Yasun E, Kang H, Erdal H, Cansiz S, Ocsoy I, Huang YF, Tan W (2013) Cancer cell sensing and therapy using affinity tag-conjugated gold nanorods. Interface Focus 3:20130006

    Article  Google Scholar 

  39. Yasun E, Li C, Barut I, Janvier D, Qiu L, Cui C, Tan W (2015) BSA modification to reduce CTAB induced nonspecificity and cytotoxicity of aptamer-conjugated gold nanorods. Nanoscale 7:10240–10248

    CAS  Article  Google Scholar 

  40. Yi Y, Wang H, Wang X, Liu Q, Ye M, Tan W (2017) A smart, photocontrollable drug release nanosystem for multifunctional synergistic cancer therapy. ACS Appl Mater Interfaces 9:5847–5854

    CAS  Article  Google Scholar 

  41. Yuan B, Jiang X, Chen Y, Guo Q, Wang K, Meng X, Huang Z, Wen X (2017) Metastatic cancer cell and tissue-specific fluorescence imaging using a new DNA aptamer developed by Cell-SELEX. Talanta 170:56–62

    CAS  Article  Google Scholar 

  42. Zelasko-Leon DC, Fuentes CM, Messersmith PB (2015) MUC1-targeted cancer cell photothermal ablation using bioinspired gold nanorods. PLoS One 10:e0128756

    Article  Google Scholar 

  43. Zhang Z, Wang J, Chen C (2013) Gold nanorods based platforms for light-mediated theranostics. Theranostics 3:223–238

    CAS  Article  Google Scholar 

  44. Zhang S, Li Y, He X, Dong S, Huang Y, Li X, Li Y, Jin C, Zhang Y, Wang Y (2014) Photothermolysis mediated by gold nanorods modified with EGFR monoclonal antibody induces Hep-2 cells apoptosis in vitro and in vivo. Int J Nanomedicine 9:1931–1946

    Google Scholar 

  45. Zhao J, Wang A, Si T, Hong JD, Li J (2019) Gold nanorods based multicompartment mesoporous silica composites as bioagents for highly efficient photothermal therapy. J Colloid Interface Sci 549:9–15

    CAS  Article  Google Scholar 

  46. Zhou F, Xing D, Ou Z, Wu B, Resasco DE, Chen WR (2009) Cancer photothermal therapy in the near-infrared region by using single-walled carbon nanotubes. J Biomed Opt 14:021009

    Article  Google Scholar 

  47. Zou L, Wang H, He B, Zeng L, Tan T, Cao H, He X, Zhang Z (2016) Current approaches of photothermal therapy in treating cancer metastasis with nanotherapeutics. Theranostics 6:762–772

    CAS  Article  Google Scholar 

Download references

Funding

This work was financially supported by grants from the Global Research Lab (GRL) Program [NRF-2013K1A1A2A02050616] and the Mid-career Researcher Program [NRF-2017R1A2B3010816] through a National Research Foundation grant funded by the Ministry of Science, ICT, and Future Planning.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Min-Gon Kim.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 1532 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Noh, Y., Kim, M., Mun, H. et al. Aptamer-based selective KB cell killing by the photothermal effect of gold nanorods. J Nanopart Res 21, 112 (2019). https://doi.org/10.1007/s11051-019-4561-y

Download citation

Keywords

  • Systematic evolution of ligands by exponential enrichment
  • KB cancer cells
  • Aptamers
  • Gold nanorods
  • Photothermal killing
  • Nanomedicine