Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-02T23:53:20.790Z Has data issue: false hasContentIssue false
  • English
  • Français

Intracellular microRNA quantification in intact cells: a novel strategy based on reduced graphene oxide-based fluorescence quenching

Published online by Cambridge University Press:  13 July 2018

Ramasamy Paulmurugan ,
Pulickel M. Ajayan ,
Dorian Liepmann  and
V. Renugopalakrishnan
Ramasamy Paulmurugan*
Affiliation:
Cellular Pathway Imaging Laboratory (CPIL), Department of Radiology, Stanford University School of Medicine, 3155 Porter Drive, Suite 2236, Palo Alto, CA 94304, USA
Pulickel M. Ajayan
Affiliation:
Department of Materials Science and Nanoengineering, Rice University, Houston, TX 77005, USA
Dorian Liepmann
Affiliation:
Department of Bioengineering, University of California, Berkeley, CA, USA
V. Renugopalakrishnan
Affiliation:
Boston Children's Hospital, Harvard Medical School, Boston, MA 02115, USA Department of Chemistry and Chemical Biology, Northeastern University, Boston, MA 02115, USA
*
Address all correspondence to Ramasamy Paulmurugan at [email protected]
Get access

Abstract

Nanomaterials have been proposed as key components in biosensing, imaging, and drug delivery since they offer distinctive advantages over conventional approaches. The unique chemical and physical properties of graphene make it possible to functionalize and develop protein transducers, therapeutic delivery vehicles, and microbial diagnostics. In this study, we evaluate reduced graphene oxide as a potential nanomaterial for quantification of microRNAs including their structural differentiation in vitro in solution and inside intact cells. Our results provide evidence for the potential use of graphene nanomaterials as a platform for developing devices that can be used for microRNA quantitation as biomarkers for clinical applications.

Type
2D Nanomaterials for Healthcare and Lab-on-a-Chip Devices Prospective Articles
Information
MRS Communications , Volume 8 , Issue 3 , September 2018 , pp. 642 - 651
Check for updates
Copyright
Copyright © Materials Research Society 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Abbasi, E., Akbarzadeh, A., Kouhi, M., and Milani, M.: Graphene: synthesis, bio-applications, and properties. Artif. Cells Nanomed. Biotechnol. 44, 150 (2016).Google Scholar
2.Yan, P., Zhang, X., Hou, M., Liu, Y., Liu, T., Liu, K., and Zhang, R.: Ultrahigh-power supercapacitors based on highly conductive graphene nanosheet/nanometer-sized carbide-derived carbon frameworks. Nanotechnology 29, 255403 (2018).Google Scholar
3.Viswanathan, S., Narayanan, T.N., Aran, K., Fink, K.D., Paredes, J., Ajayan, P.M., Filipek, S., Miszta, P., Tekin, H.C., Inci, F., Demirci, U., Li, P., Bolotin, K.I., Liepmann, D., and Renugopalakrishanan, V.: Graphene–protein field effect biosensors: glucose sensing. Materialstoday 18, 513 (2015).Google Scholar
4.Sekar, T.V., Mohanram, R.K., Foygel, K., and Paulmurugan, R.: Therapeutic evaluation of microRNAs by molecular imaging. Theranostics 3, 964 (2013).Google Scholar
5.Macfarlane, L.A. and Murphy, P.R.: MicroRNA: biogenesis, function and role in cancer. Curr. Genomics 11, 537 (2010).Google Scholar
6.Ha, M. and Kim, V.N.: Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15, 509 (2014).Google Scholar
7.Ha, T.Y.: MicroRNAs in human diseases: from cancer to cardiovascular disease. Immune. Netw. 11, 135 (2011).Google Scholar
8.Kitade, Y. and Akao, Y.: MicroRNAs and their therapeutic potential for human diseases: microRNAs, miR-143 and -145, function as anti-oncomirs and the application of chemically modified miR-143 as an anti-cancer drug. J. Pharmacol. Sci. 114, 276 (2010).Google Scholar
9.Martinez, B. and Peplow, P.V.: MicroRNAs as diagnostic markers and therapeutic targets for traumatic brain injury. Neural. Regen. Res. 12, 1749 (2017).Google Scholar
10.Hou, J., Meng, F., Chan, L.W., Cho, W.C., and Wong, S.C.: Circulating plasma microRNAs as diagnostic markers for NSCLC. Front. Genet. 7, 193 (2016).Google Scholar
11.Gustafson, D., Tyryshkin, K., and Renwick, N.: microRNA-guided diagnostics in clinical samples. Best Pract. Res. Clin. Endocrinol. Metab. 30, 563 (2016).Google Scholar
12.Madni, A., Noreen, S., Maqbool, I., Rehman, F., Batool, A., Kashif, P.M., Rehman, M., Tahir, N., and Khan, M.I.: Graphene-based nanocomposites: synthesis and their theranostic applications. J. Drug Target. 26, 1 (2018).Google Scholar
13.Jang, S.C., Kang, S.M., Lee, J.Y., Oh, S.Y., Vilian, A.E., Lee, I., Han, Y.K., Park, J.H., Cho, W.S., Roh, C., and Huh, Y.S.: Nano-graphene oxide composite for in vivo imaging. Int. J. Nanomedicine 13, 221 (2018).Google Scholar
14.Ma, C., Liu, H., Wu, K., Chen, M., Zheng, L., and Wang, J.: An exonuclease I-based quencher-free fluorescent method using DNA hairpin probes for rapid detection of microRNA. Sensors (Basel) 17 (2017).Google Scholar
15.Hasan, M.T., Senger, B.J., Mulford, P., Ryan, C., Doan, H., Gryczynski, Z., and Naumov, A.V.: Modifying optical properties of reduced/graphene oxide with controlled ozone and thermal treatment in aqueous suspensions. Nanotechnology 28, 065705 (2017).Google Scholar
16.Suvarnaphaet, P. and Pechprasarn, S.: Graphene-based materials for biosensors: a review. Sensors (Basel) 17 (2017).Google Scholar
17.Wang, L., Wu, A., and Wei, G.: Graphene-based aptasensors: from molecule-interface interactions to sensor design and biomedical diagnostics. Analyst 143, 1526 (2018).Google Scholar
18.Muchharla, B., Narayanan, T.N., Balakrishnan, K., Ajayan, P.M., and Talapatra, S.: Temperature dependent electrical transport of disordered reduced graphene oxide. 2D Mater. 1 (2014) 011008 2053-1583/14/011008 (2010).Google Scholar
19.Huang, R.C., Chiu, W.J., Li, Y.J., and Huang, C.C.: Detection of microRNA in tumor cells using exonuclease III and graphene oxide-regulated signal amplification. ACS Appl. Mater. Interfaces 6, 21780 (2014).Google Scholar
20.Akao, Y., Nakagawa, Y., Hirata, I., Iio, A., Itoh, T., Kojima, K., Nakashima, R., Kitade, Y., and Naoe, T.: Role of anti-oncomirs miR-143 and -145 in human colorectal tumors. Cancer Gene Ther. 17, 398 (2010).Google Scholar
21.Esquela-Kerscher, A. and Slack, F.J.: Oncomirs—microRNAs with a role in cancer. Nat. Rev. Cancer 6, 259 (2006).Google Scholar
22.Krutovskikh, V.A. and Herceg, Z.: Oncogenic microRNAs (OncomiRs) as a new class of cancer biomarkers. Bioessays 32, 894 (2010).Google Scholar
23.Reshmi, G. and Pillai, M.R.: Beyond HPV: oncomirs as new players in cervical cancer. FEBS Lett. 582, 4113 (2008).Google Scholar
24.Kota, J., Chivukula, R.R., O'Donnell, K.A., Wentzel, E.A., Montgomery, C.L., Hwang, H.W., Chang, T.C., Vivekanandan, P., Torbenson, M., Clark, K.R., Mendell, J.R., and Mendell, J.T.: Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137, 1005 (2009).Google Scholar
25.Liu, C., Kelnar, K., Liu, B., Chen, X., Calhoun-Davis, T., Li, H., Patrawala, L., Yan, H., Jeter, C., Honorio, S., Wiggins, J.F., Bader, A.G., Fagin, R., Brown, D., and Tang, D.G.: The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat. Med. 17, 211 (2011).Google Scholar
26.Krutzfeldt, J., Rajewsky, N., Braich, R., Rajeev, K.G., Tuschl, T., Manoharan, M., and Stoffel, M.: Silencing of microRNAs in vivo with ‘antagomirs’. Nature 438, 685 (2005).Google Scholar
27.Ross, J.S., Carlson, J.A., and Brock, G.: miRNA: the new gene silencer. Am. J. Clin. Pathol. 128, 830 (2007).Google Scholar
28.De Palma, M. and Naldini, L.: Antagonizing metastasis. Nat. Biotechnol. 28, 331 (2010).Google Scholar
29.Ma, L., Reinhardt, F., Pan, E., Soutschek, J., Bhat, B., Marcusson, E.G., Teruya-Feldstein, J., Bell, G.W., and Weinberg, R.A.: Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat. Biotechnol. 28, 341 (2010).Google Scholar
30.Devulapally, R., Foygel, K., Sekar, T.V., Willmann, J.K., and Paulmurugan, R.: Gemcitabine and antisense-microRNA co-encapsulated PLGA-PEG polymer nanoparticles for hepatocellular carcinoma therapy. ACS Appl. Mater. Interfaces 8, 33412 (2016).Google Scholar
31.Devulapally, R. and Paulmurugan, R.: Polymer nanoparticles for drug and small silencing RNA delivery to treat cancers of different phenotypes. Wiley. Interdiscip. Rev. Nanomed. Nanobiotechnol. 6, 40 (2014).Google Scholar
32.Devulapally, R., Sekar, N.M., Sekar, T.V., Foygel, K., Massoud, T.F., Willmann, J.K., and Paulmurugan, R.: Polymer nanoparticles mediated codelivery of antimiR-10b and antimiR-21 for achieving triple negative breast cancer therapy. ACS Nano 9, 2290 (2015).Google Scholar
33.Devulapally, R., Sekar, T.V., and Paulmurugan, R.: Formulation of anti-miR-21 and 4-hydroxytamoxifen co-loaded biodegradable polymer nanoparticles and their antiproliferative effect on breast cancer cells. Mol. Pharm. 12, 2080 (2015).Google Scholar
34.Ananta, J.S., Paulmurugan, R., and Massoud, T.F.: Tailored nanoparticle codelivery of antimiR-21 and antimiR-10b augments glioblastoma cell kill by temozolomide: toward a “personalized” anti-microRNA therapy. Mol. Pharm. 13, 3164 (2016).Google Scholar
35.Ananta, J.S., Paulmurugan, R., and Massoud, T.F.: Temozolomide-loaded PLGA nanoparticles to treat glioblastoma cells: a biophysical and cell culture evaluation. Neurol. Res. 38, 51 (2016).Google Scholar
36.Ananta, J.S., Paulmurugan, R., and Massoud, T.F.: Nanoparticle-delivered antisense microrna-21 enhances the effects of temozolomide on glioblastoma cells. Mol. Pharm. 12, 4509 (2015).Google Scholar
37.Cheng, C.J., Bahal, R., Babar, I.A., Pincus, Z., Barrera, F., Liu, C., Svoronos, A., Braddock, D.T., Glazer, P.M., Engelman, D.M., Saltzman, W.M., and Slack, F.J.: MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature 518, 107 (2015).Google Scholar
38.Asangani, I.A., Rasheed, S.A., Nikolova, D.A., Leupold, J.H., Colburn, N.H., Post, S., and Allgayer, H.: MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27, 2128 (2008).Google Scholar
39.Chan, J.A., Krichevsky, A.M., and Kosik, K.S.: MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 65, 6029 (2005).Google Scholar
40.Cheng, A.M., Byrom, M.W., Shelton, J., and Ford, L.P.: Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res. 33, 1290 (2005).Google Scholar
41.Loffler, D., Brocke-Heidrich, K., Pfeifer, G., Stocsits, C., Hackermuller, J., Kretzschmar, A.K., Burger, R., Gramatzki, M., Blumert, C., Bauer, K., Cvijic, H., Ullmann, A.K., Stadler, P.F., and Horn, F.: Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 110, 1330 (2007).Google Scholar
42.Papagiannakopoulos, T., Shapiro, A., and Kosik, K.S.: MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res. 68, 8164 (2008).Google Scholar
43.Zhang, Z., Li, Z., Gao, C., Chen, P., Chen, J., Liu, W., Xiao, S., and Lu, H.: miR-21 plays a pivotal role in gastric cancer pathogenesis and progression. Lab. Invest. 88, 1358 (2008).Google Scholar
44.Zhu, S., Wu, H., Wu, F., Nie, D., Sheng, S., and Mo, Y.Y.: MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res. 18, 350 (2008).Google Scholar