Deep tissue localization and sensing using optical microcavity probes.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
11 03 2022
11 03 2022
Historique:
received:
16
08
2021
accepted:
15
02
2022
entrez:
12
3
2022
pubmed:
13
3
2022
medline:
6
4
2022
Statut:
epublish
Résumé
Optical microcavities and microlasers were recently introduced as probes inside living cells and tissues. Their main advantages are spectrally narrow emission lines and high sensitivity to the environment. Despite numerous novel methods for optical imaging in strongly scattering biological tissues, imaging at single-cell resolution beyond the ballistic light transport regime remains very challenging. Here, we show that optical microcavity probes embedded inside cells enable three-dimensional localization and tracking of individual cells over extended time periods, as well as sensing of their environment, at depths well beyond the light transport length. This is achieved by utilizing unique spectral features of the whispering-gallery modes, which are unaffected by tissue scattering, absorption, and autofluorescence. In addition, microcavities can be functionalized for simultaneous sensing of various parameters, such as temperature or pH value, which extends their versatility beyond the capabilities of standard fluorescent labels.
Identifiants
pubmed: 35277496
doi: 10.1038/s41467-022-28904-6
pii: 10.1038/s41467-022-28904-6
pmc: PMC8917156
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1269Informations de copyright
© 2022. The Author(s).
Références
Jacques, S. L. Optical properties of biological tissues: a review. Phys. Med. Biol. 58, R37–R61 (2013).
pubmed: 23666068
doi: 10.1088/0031-9155/58/11/R37
Ntziachristos, V. Going deeper than microscopy: the optical imaging frontier in biology. Nat. Methods 7, 603–614 (2010).
pubmed: 20676081
doi: 10.1038/nmeth.1483
Theer, P. & Denk, W. On the fundamental imaging-depth limit in two-photon microscopy. J. Opt. Soc. Am. 23, 3139–3149 (2006).
doi: 10.1364/JOSAA.23.003139
Tkaczyk, E. R. Innovations and developments in dermatologic non-invasive optical imaging and potential clinical applications. Acta Derm-Venereol 5 (2017).
Yoon, S. et al. Deep optical imaging within complex scattering media. Nat. Rev. Phys.1–18 (2020).
Wang, L. V. Photoacoustic imaging and spectroscopy (CRC Press, 2017).
Ruan, H., Liu, Y., Xu, J., Huang, Y. & Yang, C. Fluorescence imaging through dynamic scattering media with speckle-encoded ultrasound-modulated light correlation. Nat. Photonics 14, 511–516 (2020).
doi: 10.1038/s41566-020-0630-0
Jiang, H. Diffuse optical tomography: principles and applications (CRC Press, 2018).
Yu, H. et al. Recent advances in wavefront shaping techniques for biomedical applications. Curr. Appl. Phys. 15, 632–641 (2015).
doi: 10.1016/j.cap.2015.02.015
Velasco, M. G. M. et al. 3d super-resolution deep-tissue imaging in living mice. Optica 8, 442–450 (2021).
pubmed: 34239948
pmcid: 8243577
doi: 10.1364/OPTICA.416841
Maric, D. et al. Whole-brain tissue mapping toolkit using large-scale highly multiplexed immunofluorescence imaging and deep neural networks. Nat. Commun. 12, 1–12 (2021).
doi: 10.1038/s41467-021-21735-x
Ntziachristos, V., Tung, C.-H., Bremer, C. & Weissleder, R. Fluorescence molecular tomography resolves protease activity in vivo. Nat. Med. 8, 757–761 (2002).
pubmed: 12091907
doi: 10.1038/nm729
Stuker, F., Ripoll, J. & Rudin, M. Fluorescence molecular tomography: principles and potential for pharmaceutical research. Pharmaceutics 3, 229–274 (2011).
pubmed: 24310495
pmcid: 3864234
doi: 10.3390/pharmaceutics3020229
Ozturk, M. S. et al. Intravital mesoscopic fluorescence molecular tomography allows non-invasive in vivo monitoring and quantification of breast cancer growth dynamics. Commun. Biol. 4, 1–11 (2021).
doi: 10.1038/s42003-021-02063-8
Yang, F. et al. Improving mesoscopic fluorescence molecular tomography via preconditioning and regularization. Biomed. Opt. Express 9, 2765–2778 (2018).
pubmed: 30258689
pmcid: 6154183
doi: 10.1364/BOE.9.002765
Dang, X. et al. Deep-tissue optical imaging of near cellular-sized features. Sci. Rep. 9, 1–12 (2019).
doi: 10.1038/s41598-019-39502-w
Moretti, C. & Gigan, S. Readout of fluorescence functional signals through highly scattering tissue. Nat. Photonics 14, 361–364 (2020).
doi: 10.1038/s41566-020-0612-2
Welsher, K. et al. A route to brightly fluorescent carbon nanotubes for near-infrared imaging in mice. Nat. Nanotechnol. 4, 773–780 (2009).
pubmed: 19893526
pmcid: 2834239
doi: 10.1038/nnano.2009.294
Fan, X. & Yun, S.-H. The potential of optofluidic biolasers. Nat. Methods 11, 141–147 (2014).
pubmed: 24481219
pmcid: 4162132
doi: 10.1038/nmeth.2805
Martino, N. et al. Wavelength-encoded laser particles for massively multiplexed cell tagging. Nat. Photonics 13, 720–727 (2019).
pubmed: 32231707
pmcid: 7104740
doi: 10.1038/s41566-019-0489-0
Schubert, M. et al. Lasing within live cells containing intracellular optical microresonators for barcode-type cell tagging and tracking. Nano Lett. 15, 5647–5652 (2015).
pubmed: 26186167
doi: 10.1021/acs.nanolett.5b02491
Toropov, N. & Vollmer, F., Whispering-gallery microlasers for cell tagging and barcoding: the prospects for in vivo biosensing. Light Sci. Appl. 10, 77 (2021).
pubmed: 33854030
pmcid: 8046988
doi: 10.1038/s41377-021-00517-6
Tang, S.-J. et al. Laser particles with omnidirectional emission for cell tracking. Light Sci. Appl. 10, 1–11 (2021).
Toropov, N. et al. Review of biosensing with whispering-gallery mode lasers. Light Sci. Appl. 10, 1–19 (2021).
doi: 10.1038/s41377-021-00471-3
Schubert, M. et al. Monitoring contractility in cardiac tissue with cellular resolution using biointegrated microlasers. Nat. Photonics 14, 452–458 (2020).
doi: 10.1038/s41566-020-0631-z
Humar, M. & Yun, S. H. Intracellular microlasers. Nat. Photonics 9, 572–576 (2015).
pubmed: 26417383
pmcid: 4583142
doi: 10.1038/nphoton.2015.129
Cho, S., Humar, M., Martino, N. & Yun, S. H. Laser particle stimulated emission microscopy. Phys. Rev. Lett. 117, 193902 (2016).
pubmed: 27858427
pmcid: 5436487
doi: 10.1103/PhysRevLett.117.193902
Fernandez-Rosas, E. et al. Intracellular polysilicon barcodes for cell tracking. Small 5, 2433–2439 (2009).
pubmed: 19670393
doi: 10.1002/smll.200900733
Gratton, S. E. et al. The effect of particle design on cellular internalization pathways. Proc. Natl. Acad. Sci. U.S.A 105, 11613–11618 (2008).
pubmed: 18697944
pmcid: 2575324
doi: 10.1073/pnas.0801763105
Fernández-Rosas, E. et al. Internalization and cytotoxicity analysis of silicon-based microparticles in macrophages and embryos. Biomed. Microdevices 12, 371–379 (2010).
pubmed: 20069375
doi: 10.1007/s10544-009-9393-6
Humar, M., Dobravec, A., Zhao, X. & Yun, S. H. Biomaterial microlasers implantable in the cornea, skin, and blood. Optica 4, 1080–1085 (2017).
pubmed: 30333986
pmcid: 6188636
doi: 10.1364/OPTICA.4.001080
Matsko, A. B. & Ilchenko, V. S. Optical resonators with whispering gallery modes I: Basics. IEEE J. Sel. Top. Quant. 12, 3–14 (2006).
doi: 10.1109/JSTQE.2005.862952
Gorodetsky, M. L. & Fomin, A. E. Geometrical theory of whispering-gallery modes. IEEE J. Sel. Top. Quant. 12, 33–39 (2006).
doi: 10.1109/JSTQE.2005.862954
Schubert, M. et al. Lasing in live mitotic and non-phagocytic cells by efficient delivery of microresonators. Sci. Rep. 7, 1–9 (2017).
doi: 10.1038/srep40877
Humar, M., Upadhya, A. & Yun, S. H. Spectral reading of optical resonance-encoded cells in microfluidics. Lab. Chip. 17, 2777–2784 (2017).
pubmed: 28686280
pmcid: 5555601
doi: 10.1039/C7LC00220C
Coclite, A. M. et al. 25th anniversary article: CVD polymers: a new paradigm for surface modification and device fabrication. Adv. Mater. 25, 5392–5423 (2013).
pubmed: 24115244
doi: 10.1002/adma.201301878
Muralter, F., Perrotta, A., Werzer, O. & Coclite, A. M. Interlink between tunable material properties and thermoresponsiveness of cross-linked poly (N-vinylcaprolactam) thin films deposited by initiated chemical vapor deposition. Macromolecules 52, 6817–6824 (2019).
pubmed: 31579141
pmcid: 6764023
doi: 10.1021/acs.macromol.9b01364
Ghasemi-Mobarakeh, L. et al. Manipulating drug release from tridimensional porous substrates coated by initiated chemical vapor deposition. J. Appl. Polym. Sci. 136, 47858 (2019).
doi: 10.1002/app.47858
Thews, O. & Riemann, A. Tumor ph and metastasis: a malignant process beyond hypoxia. Cancer Metast. Rev. 38, 113–129 (2019).
doi: 10.1007/s10555-018-09777-y
Horton, N. G. et al. In vivo three-photon microscopy of subcortical structures within an intact mouse brain. Nat. Photonics 7, 205–209 (2013).
pmcid: 3864872
doi: 10.1038/nphoton.2012.336
Fikouras, A. H. et al. Non-obstructive intracellular nanolasers. Nat. Commun. 9, 1–7 (2018).
doi: 10.1038/s41467-018-07248-0
Liu, Y. et al. Controlled assembly of upconverting nanoparticles for low-threshold microlasers and their imaging in scattering media. ACS Nano 14, 1508–1519 (2020).
pubmed: 32053350
doi: 10.1021/acsnano.9b06102
Galanzha, E. I. et al. Spaser as a biological probe. Nat. Commun. 8, 15528 (2017).
pubmed: 28593987
pmcid: 5472166
doi: 10.1038/ncomms15528
Bulte, J. W. & Daldrup-Link, H. E. Clinical tracking of cell transfer and cell transplantation: trials and tribulations. Radiology 289, 604–615 (2018).
pubmed: 30299232
doi: 10.1148/radiol.2018180449
Manzo, M., Cavazos, O., Ramirez-Cedillo, E. & Siller, H. R. Embedded spherical microlasers for in vivo diagnostic biomechanical performances. J. Eng. Sci. Med. Diagn. Therapy 3, 044504 (2020).
Pirnat, G. & Humar, M., Whispering gallery-mode microdroplet tensiometry. Adv. Photonics Res. 2, 2100129 (2021).
doi: 10.1002/adpr.202100129
de Bruin, D. M. M. et al. Optical phantoms of varying geometry based on thin building blocks with controlled optical properties. J. Biomed. Opt. 15, 025001 (2010).
pubmed: 20459242
doi: 10.1117/1.3369003
Prahl, S. et al. Mie scattering calculator (2007). https://omlc.org/calc/mie_calc.html .
Cohoon, D. An exact solution of mie type for scattering by a multilayer anisotropic sphere. J. Electromagn. Wave. 3, 421–448 (1989).
doi: 10.1163/156939389X00142
Taddeucci, A., Martelli, F., Barilli, M., Ferrari, M. & Zaccanti, G. Optical properties of brain tissue. J. Biomed. Opt. 1, 117–124 (1996).
pubmed: 23014652
doi: 10.1117/12.227816
Ranacher, C. et al. Layered nanostructures in proton conductive polymers obtained by initiated chemical vapor deposition. Macromolecules 48, 6177–6185 (2015).
doi: 10.1021/acs.macromol.5b01145