Spatial tumor biopsy with fluorescence PCR microneedle array
-
GRAPHICAL ABSTRACT
DownLoad:
Full size image
-
PUBLIC SUMMARY
- ■ Bioinspired microneedle platform with heterogeneous wettability is fabricated.
- ■ Hydrophobic nanoparticle-assembled substrate secludes each needle peak.
- ■ Graphene aerogel hybrid needle peaks collect biomarkers on tissue in a 3D manner.
- ■ PCR reactions are directly conducted on the platform to detect clinical specimens.
-
ABSTRACT
Biopsy is the gold standard for tumor diagnosis, as this technology provides highly detailed and reliable information on tumorigenesis and progression. Resembling the discrete wettability of desert beetles, in this study, a fluorescence polymerase chain reaction (F-PCR) microneedle array (MNA) platform is developed for efficient spatial tumor biopsy. This MNA is fabricated by the coupled strategies of bottom-up self-assembly and top-down photolithography; it comprises a hydrophobic silica nanoparticle-assembled substrate and graphene aerogel-hydrogel hybrid microneedle peaks. Benefitting from the hydrophilicity and absorption capacity of its graphene hybrid microneedle peaks, MNA can easily penetrate tissue specimens and collect tumor nucleic acid biomarkers stereoscopically. In addition, because of the discrete wettability of the platform, both tissue fluids and PCR liquids can be easily removed from the substrate, and each microneedle peak is similar to an independent island for directly conducting F-PCR reactions for tumor marker discovery. Based on these advantages, the F-PCR-MNA platform is demonstrated to be ideal for detecting DNA biomarkers of lung carcinoma in standard solutions, mouse tissue samples, and clinical specimens, thus indicating its practical potential as an innovative tumor biopsy system. -
-
REFERENCES
[1] Wu, L., Ishigaki, Y., Hu, Y., et al. (2020). H2S-activatable near-infrared afterglow luminescent probes for sensitive molecular imaging in vivo. Nat. Commun. 11, 446. [2] Chen, J., Jiang, Z., Zhang, Y.S., et al. (2021). Smart transformable nanoparticles for enhanced tumor theranostics. Appl. Phys. Rev. 8, 041321. [3] Liu, Y., Wang, J., Xiong, Q., et al. (2021). Nano-bio interactions in cancer: from therapeutics delivery to early detection. Acc. Chem. Res. 54, 291-301. [4] Wu, D., Chi, J., Zhang, M., et al. (2022). Water-dispersing perovskite probes for the rapid imaging of glioma cells. Adv. Opt. Mater. 10, 2101835. [5] Zhang, Y., Tu, J., Wang, D., et al. (2018). Programmable and multifunctional DNA-based materials for biomedical applications. Adv. Mater. 30, 1703658. [6] Crosby, D., Bhatia, S., Brindle, K.M., et al. (2022). Early detection of cancer. Science 375, eaay9040. [7] Zhao, M., Mi, D., Ferdows, B.E., et al. (2022). State-of-the-art nanotechnologies for the detection, recovery, analysis and elimination of liquid biopsy components in cancer. Nano Today 42, 101361. [8] Kim, E.S., Velcheti, V., Mekhail, T., et al. (2022). Blood-based tumor mutational burden as a biomarker for atezolizumab in non-small cell lung cancer: the phase 2 B-F1RST trial. Nat. Med. 28, 939-945. [9] Ji, X., Ge, L., Liu, C., et al. (2021). Capturing functional two-dimensional nanosheets from sandwich-structure vermiculite for cancer theranostics. Nat. Commun. 12, 1124. [10] Haddad, T.S., Friedl, P., Farahani, N., et al. (2021). Tutorial: Methods for three-dimensional visualization of archival tissue material. Nat. Protoc. 16, 4945-4962. [11] He, J., Chen, C., Chen, L., et al. (2022). Honeycomb-like hydrogel microspheres for 3D bulk construction of tumor models. Research 2022, 9809763. [12] Zhao, T., Chiang, Z.D., Morriss, J.W., et al. (2022). Spatial genomics enables multi-modal study of clonal heterogeneity in tissues. Nature 601, 85-91. [13] Patel, K.B., Liang, W., Casper, M.J., et al. (2022). High-speed light-sheet microscopy for the in-situ acquisition of volumetric histological images of living tissue. Nat. Biomed. Eng. 6, 569-583. [14] Balaur, E., O’ Toole, S., Spurling, A.J., et al. (2021). Colorimetric histology using plasmonically active microscope slides. Nature 598, 65-71. [15] Zhang, D., Deng, Y., Kukanja, P., et al. (2023). Spatial epigenome–transcriptome co-profiling of mammalian tissues. Nature 616, 113-122. [16] Wirth, J., Huber, N., Yin, K., et al. (2023). Spatial transcriptomics using multiplexed deterministic barcoding in tissue. Nat. Commun. 14, 1523. [17] Jamaledin, R., Yiu, C.K.Y., Zare, E.N., et al. (2020). Advances in antimicrobial microneedle patches for combating infections. Adv. Mater. 32, 2002129. [18] Zhang, X., Chen, G., Bian, F., et al. (2019). Encoded microneedle arrays for detection of skin interstitial fluid biomarkers. Adv. Mater. 31, 1902825. [19] Yang, J., Zhang, H., Hu, T., et al. (2021). Recent advances of microneedles used towards stimuli-responsive drug delivery, disease theranostics, and bioinspired applications. Chem. Eng. J. 426, 130561. [20] Wang, Z., Luan, J., Seth, A., et al. (2021). Microneedle patch for the ultrasensitive quantification of protein biomarkers in interstitial fluid. Nat. Biomed. Eng. 5, 64-76. [21] Yi, K., Wang, Y., Shi, K., et al. (2021). Aptamer-decorated porous microneedles arrays for extraction and detection of skin interstitial fluid biomarkers. Biosens. Bioelectron. 190, 113404. [22] Keyvani, F., Zheng, H., Kaysir, M.R., et al. (2023). A hydrogel microneedle assay combined with nucleic acid probes for on-site detection of small molecules and proteins. Angew. Chem. Int. Ed. 62, e202301624. [23] Tehrani, F., Teymourian, H., Wuerstle, B., et al. (2022). An integrated wearable microneedle array for the continuous monitoring of multiple biomarkers in interstitial fluid. Nat. Biomed. Eng. 6, 1214-1224. [24] Paul, R., Ostermann, E., Chen, Y., et al. (2021). Integrated microneedle-smartphone nucleic acid amplification platform for in-field diagnosis of plant diseases. Biosens. Bioelectron. 187, 113312. [25] Chen, L., Ding, J., Yuan, H., et al. (2022). Deep-dLAMP: Deep learning-enabled polydisperse emulsion-based digital loop-mediated isothermal amplification. Adv. Sci. 9, 2105450. [26] Sun, C., Liu, L., Pérez, L., et al. (2022). Droplet-microfluidics-assisted sequencing of HIV proviruses and their integration sites in cells from people on antiretroviral therapy. Nat. Biomed. Eng. 6, 1004-1012. [27] Al Sulaiman, D., Juthani, N., and Doyle, P.S. (2022). Quantitative and multiplex detection of extracellular vesicle-derived microRNA via rolling circle amplification within encoded hydrogel microparticles. Adv. Healthc. Mater. 11, 2102332. [28] Song, P., Wu, L.R., Yan, Y.H., et al. (2022). Limitations and opportunities of technologies for the analysis of cell-free DNA in cancer diagnostics. Nat. Biomed. Eng. 6, 232-245. [29] Wang, Z., and Cui, W. (2020). CRISPR-Cas system for biomedical diagnostic platforms. View 1, 20200008. [30] Wei, Q., Arami, H., Santos, H.A., et al. (2021). Intraoperative assessment and photothermal ablation of the tumor margins using gold nanoparticles. Adv. Sci. 8, 2002788. [31] Herberts, C., Annala, M., Sipola, J., et al. (2022). Deep whole-genome ctDNA chronology of treatment-resistant prostate cancer. Nature 608, 199-208. [32] Zhang, X., Sun, L., Wang, Y., et al. (2019). Multibioinspired slippery surfaces with wettable bump arrays for droplets pumping. P. Natl. Acad. Sci. USA 116, 20863-20868. [33] Zhang, H., Zhao, G., Wu, S., et al. (2021). Solar anti-icing surface with enhanced condensate self-removing at extreme environmental conditions. P. Natl. Acad. Sci. USA 118, e2100978118. [34] Li, H., Li, A., Zhao, Z., et al. (2021). Precise droplet manipulation based on surface heterogeneity. Acc. Mater. Res. 2, 230-241. [35] Bian, F., Sun, L., Cai, L., et al. (2020). Bioinspired MXene-integrated colloidal crystal arrays for multichannel bioinformation coding. P. Natl. Acad. Sci. USA 117, 22736-22742. [36] Pang, K., Song, X., Xu, Z., et al. (2020). Hydroplastic foaming of graphene aerogels and artificially intelligent tactile sensors. Sci. Adv. 6, eabd4045. [37] Wang, B., Zhang, S., Meng, J., et al. (2021). Evaporation-Induced rGO coatings for highly sensitive and non-invasive diagnosis of prostate cancer in the PSA gray zone. Adv. Mater. 33, 2103999. [38] Wu, S., Liang, Z., Li, Y., et al. (2022). Transparent, photothermal, and icephobic surfaces via layer-by-layer assembly. Adv. Sci. 9, 2105986. [39] Liu, F., Yang, Y., Wan, X., et al. (2022). Space-confinment-enhanced fluorescence detection of DNA on hydrogel particles array. ACS Nano 16, 6266-6273. [40] Chaudhuri, A.A., Chabon, J.J., Lovejoy, A.F., et al. (2017). Early detection of molecular residual disease in localized lung cancer by circulating. Cancer Discov. 7, 1394-1403. [41] Mathios, D., Johansen, J.S., Cristiano, S., et al. (2021). Detection and characterization of lung cancer using cell-free DNA fragmentomes. Nat. Commun. 12, 5060. -
ABOUT THIS ARTICLE
Cite this article:
Xiaoxuan Zhang, Guopu Chen, Yu Wang, Yuanjin Zhao. Spatial tumor biopsy with fluorescence PCR microneedle array[J]. The Innovation, 2024, 5(1). https://doi.org/10.1016/j.xinn.2023.100538
Welcome!
To request copyright permission to republish or share portions of our works, please visit Copyright Clearance Center's (CCC) Marketplace website at marketplace.copyright.com.
Export File
Citation
Xiaoxuan Zhang, Guopu Chen, Yu Wang, Yuanjin Zhao. Spatial tumor biopsy with fluorescence PCR microneedle array[J]. The Innovation, 2024, 5(1). https://doi.org/10.1016/j.xinn.2023.100538
Format
Content
-
Figure 1.
Schematic illustrations of procedures of the spatial tumor biopsy by the F-PCR-MNA
-
Figure 2.
Characterization and properties of the MNA
-
Figure 3.
DNA capture and detection abilities of MNAs
-
Figure 4.
In vivo detection of mouse tissue samples
-
Figure 5.
In vivo detection of clinical patient specimens
