Targeted multicolor in vivo imaging over 1,000 nm enabled by nonamethine cyanines.
Journal
Nature methods
ISSN: 1548-7105
Titre abrégé: Nat Methods
Pays: United States
ID NLM: 101215604
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
received:
11
11
2020
accepted:
05
01
2022
pubmed:
2
3
2022
medline:
28
4
2022
entrez:
1
3
2022
Statut:
ppublish
Résumé
Recent progress has shown that using wavelengths between 1,000 and 2,000 nm, referred to as the shortwave-infrared or near-infrared (NIR)-II range, can enable high-resolution in vivo imaging at depths not possible with conventional optical wavelengths. However, few bioconjugatable probes of the type that have proven invaluable for multiplexed imaging in the visible and NIR range are available for imaging these wavelengths. Using rational design, we have generated persulfonated indocyanine dyes with absorbance maxima at 872 and 1,072 nm through catechol-ring and aryl-ring fusion, respectively, onto the nonamethine scaffold. Multiplexed two-color and three-color in vivo imaging using monoclonal antibody and dextran conjugates in several tumor models illustrate the benefits of concurrent labeling of the tumor and healthy surrounding tissue and lymphatics. These efforts are enabled by complementary advances in a custom-built NIR/shortwave-infrared imaging setup and software package for multicolor real-time imaging.
Identifiants
pubmed: 35228725
doi: 10.1038/s41592-022-01394-6
pii: 10.1038/s41592-022-01394-6
doi:
Substances chimiques
Antibodies, Monoclonal
0
Fluorescent Dyes
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, N.I.H., Intramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
353-358Subventions
Organisme : NCI NIH HHS
ID : HHSN261200800001E
Pays : United States
Informations de copyright
© 2022. This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.
Références
Nguyen, Q. T. & Tsien, R. Y. Fluorescence-guided surgery with live molecular navigation–a new cutting edge. Nat. Rev. Cancer 13, 653–662 (2013).
pubmed: 23924645
pmcid: 4427343
doi: 10.1038/nrc3566
Salo, D., Zhang, H., Kim, D. M. & Berezin, M. Y. Multispectral measurement of contrast in tissue-mimicking phantoms in near-infrared spectral range of 650 to 1,600 nm. J. Biomed. Opt. 19, 086008 (2014).
pubmed: 25104414
pmcid: 4407673
doi: 10.1117/1.JBO.19.8.086008
Carr, J. A. et al. Absorption by water increases fluorescence image contrast of biological tissue in the shortwave infrared. Proc. Natl Acad. Sci. USA 115, 9080–9085 (2018).
pubmed: 30150372
pmcid: 6140498
doi: 10.1073/pnas.1803210115
Pittet, M. J. & Weissleder, R. Intravital imaging. Cell 147, 983–991 (2011).
pubmed: 22118457
doi: 10.1016/j.cell.2011.11.004
Zhu, B., Kwon, S., Rasmussen, J. C., Litorja, M. & Sevick-Muraca, E. M. Comparison of NIR versus SWIR fluorescence image device performance using working standards calibrated with SI units. IEEE Trans. Med. Imaging 39, 944–951 (2020).
pubmed: 31478842
doi: 10.1109/TMI.2019.2937760
Thimsen, E., Sadtler, B. & Berezin, M. Y. Shortwave-infrared (SWIR) emitters for biological imaging: a review of challenges and opportunities. Nanophotonics 6, 1043–1054 (2017).
doi: 10.1515/nanoph-2017-0039
Zhu, S., Tian, R., Antaris, A. L., Chen, X. & Dai, H. Near-infrared-II molecular dyes for cancer imaging and surgery. Adv. Mater. 31, e1900321 (2019).
pubmed: 31025403
pmcid: 6555689
doi: 10.1002/adma.201900321
Hong, G. S. et al. Multifunctional in vivo vascular imaging using near-infrared II fluorescence. Nat. Med. 18, 1841–1846 (2012).
pmcid: 3595196
doi: 10.1038/nm.2995
Hong, G. S. et al. Through-skull fluorescence imaging of the brain in a new near-infrared window. Nat. Photonics 8, 723–730 (2014).
pubmed: 27642366
pmcid: 5026222
doi: 10.1038/nphoton.2014.166
Franke, D. et al. Continuous injection synthesis of indium arsenide quantum dots emissive in the short-wavelength infrared. Nat. Commun. 7, 12749 (2016).
pubmed: 27834371
pmcid: 5114595
doi: 10.1038/ncomms12749
Bruns, O. T. et al. Next-generation in vivo optical imaging with short-wave infrared quantum dots. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-017-0056 (2017).
Liu, Q. et al. Sub-10 nm hexagonal lanthanide-doped NaLuF4 upconversion nanocrystals for sensitive bioimaging in vivo. J. Am. Chem. Soc. 133, 17122–17125 (2011).
pubmed: 21957992
doi: 10.1021/ja207078s
Chen, Y. et al. Shortwave infrared in vivo imaging with gold nanoclusters. Nano Lett. 17, 6330–6334 (2017).
pubmed: 28952734
pmcid: 5902176
doi: 10.1021/acs.nanolett.7b03070
Starosolski, Z. et al. Indocyanine green fluorescence in second near-infrared (NIR-II) window. PLoS ONE 12, e0187563 (2017).
pubmed: 29121078
pmcid: 5679521
doi: 10.1371/journal.pone.0187563
Carr, J. A. et al. Shortwave infrared fluorescence imaging with the clinically approved near-infrared dye indocyanine green. Proc. Natl Acad. Sci. USA 115, 4465–4470 (2018).
pubmed: 29626132
pmcid: 5924901
doi: 10.1073/pnas.1718917115
Antaris, A. L. et al. A small-molecule dye for NIR-II imaging. Nat. Mater. https://doi.org/10.1038/nmat4476 (2015).
Wan, H. et al. A bright organic NIR-II nanofluorophore for three-dimensional imaging into biological tissues. Nat. Commun. 9, 1171 (2018).
pubmed: 29563581
pmcid: 5862886
doi: 10.1038/s41467-018-03505-4
Godard, A. et al. Water-soluble Aza-BODIPYs: biocompatible organic dyes for high contrast in vivo NIR-II imaging. Bioconjug. Chem. 31, 1088–1092 (2020).
pubmed: 32227983
doi: 10.1021/acs.bioconjchem.0c00175
Swamy, M. M. M., Murai, Y., Monde, K., Tsuboi, S. & Jin, T. Shortwave-infrared fluorescent molecular imaging probes based on pi-conjugation extended indocyanine green. Bioconjug. Chem. 32, 1541–1547 (2021).
pubmed: 34309379
doi: 10.1021/acs.bioconjchem.1c00253
Waggoner, A. Fluorescent labels for proteomics and genomics. Curr. Opin. Chem. Biol. 10, 62–66 (2006).
pubmed: 16418012
doi: 10.1016/j.cbpa.2006.01.005
Levitus, M. & Ranjit, S. Cyanine dyes in biophysical research: the photophysics of polymethine fluorescent dyes in biomolecular environments. Q. Rev. Biophys. 44, 123–151 (2011).
pubmed: 21108866
doi: 10.1017/S0033583510000247
Sauer, M. & Heilemann, M. Single-molecule localization microscopy in eukaryotes. Chem. Rev. 117, 7478–7509 (2017).
pubmed: 28287710
doi: 10.1021/acs.chemrev.6b00667
Jradi, F. M. & Lavis, L. D. Chemistry of photosensitive fluorophores for single-molecule localization microscopy. ACS Chem. Biol. 14, 1077–1090 (2019).
pubmed: 30997987
doi: 10.1021/acschembio.9b00197
Gorka, A. P., Nani, R. R. & Schnermann, M. J. Cyanine polyene reactivity: scope and biomedical applications. Org. Biomol. Chem. 13, 7584–7598 (2015).
pubmed: 26052876
pmcid: 7780248
doi: 10.1039/C5OB00788G
Hernot, S., van Manen, L., Debie, P., Mieog, J. S. D. & Vahrmeijer, A. L. Latest developments in molecular tracers for fluorescence image-guided cancer surgery. Lancet Oncol. 20, e354–e367 (2019).
pubmed: 31267970
doi: 10.1016/S1470-2045(19)30317-1
Barth, C. W. & Gibbs, S. L. Fluorescence image-guided surgery–a perspective on contrast agent development. Proc. SPIE Int. Soc. Opt. Eng. https://doi.org/10.1117/12.2545292 (2020).
Feng, Z. et al. Excretable IR-820 for in vivo NIR-II fluorescence cerebrovascular imaging and photothermal therapy of subcutaneous tumor. Theranostics 9, 5706–5719 (2019).
pubmed: 31534513
pmcid: 6735390
doi: 10.7150/thno.31332
Wu, D. et al. Extrahepatic cholangiography in near-infrared II window with the clinically approved fluorescence agent indocyanine green: a promising imaging technology for intraoperative diagnosis. Theranostics 10, 3636–3651 (2020).
pubmed: 32206113
pmcid: 7069080
doi: 10.7150/thno.41127
Zhu, S. et al. Near-infrared-II (NIR-II) bioimaging via off-peak NIR-I fluorescence emission. Theranostics 8, 4141–4151 (2018).
pubmed: 30128042
pmcid: 6096392
doi: 10.7150/thno.27995
Hu, Z. et al. First-in-human liver-tumour surgery guided by multispectral fluorescence imaging in the visible and near-infrared-I/II windows. Nat. Biomed. Eng. 4, 259–271 (2020).
pubmed: 31873212
doi: 10.1038/s41551-019-0494-0
Wang, S. et al. Anti-quenching NIR-II molecular fluorophores for in vivo high-contrast imaging and pH sensing. Nat. Commun. 10, 1058 (2019).
pubmed: 30837470
pmcid: 6401027
doi: 10.1038/s41467-019-09043-x
Cosco, E. D. et al. Flavylium polymethine fluorophores for near- and shortwave infrared imaging. Angew. Chem. Int. Ed. Engl. 56, 13126–13129 (2017).
pubmed: 28806473
doi: 10.1002/anie.201706974
Cosco, E. D. et al. Shortwave infrared polymethine fluorophores matched to excitation lasers enable noninvasive, multicolour in vivo imaging in real time. Nat. Chem. https://doi.org/10.1038/s41557-020-00554-5 (2020).
Li, B., Lu, L., Zhao, M., Lei, Z. & Zhang, F. An efficient 1,064-nm NIR-II excitation fluorescent molecular dye for deep-tissue high-resolution dynamic bioimaging. Angew. Chem. Int. Ed. Engl. 57, 7483–7487 (2018).
Bricks, J. L., Kachkovskii, A. D., Slominskii, Y. L., Gerasov, A. O. & Popov, S. V. Molecular design of near-infrared polymethine dyes: a review. Dyes Pigm. 121, 238–255 (2015).
doi: 10.1016/j.dyepig.2015.05.016
Gorka, A. P., Nani, R. R. & Schnermann, M. J. Harnessing cyanine reactivity for optical imaging and drug delivery. Acc. Chem. Res. 51, 3226–3235 (2018).
pubmed: 30418020
doi: 10.1021/acs.accounts.8b00384
Friedman, H. C. et al. Establishing design principles for emissive organic SWIR chromophores from energy gap laws. Chem. https://doi.org/10.1016/j.chempr.2021.09.001 (2021).
Cosco, E. D., Lim, I. & Sletten, E. M. Photophysical properties of indocyanine green in the shortwave infrared region. ChemPhotoChem https://doi.org/10.1002/cptc.202100045 (2021).
Nani, R. R., Kelley, J. A., Ivanic, J. & Schnermann, M. J. Reactive species involved in the regioselective photooxidation of heptamethine cyanines. Chem. Sci. 6, 6556–6563 (2015).
pubmed: 26508998
pmcid: 4618397
doi: 10.1039/C5SC02396C
Stackova, L. et al. Deciphering the structure-property relations in substituted heptamethine cyanines. J. Org. Chem. 85, 9776–9790 (2020).
pubmed: 32697591
doi: 10.1021/acs.joc.0c01104
Luciano, M. P. et al. A nonaggregating heptamethine cyanine for building brighter labeled biomolecules. ACS Chem. Biol. 14, 934–940 (2019).
pubmed: 31030512
pmcid: 6528163
doi: 10.1021/acschembio.9b00122
Pauli, J. et al. Suitable labels for molecular imaging—influence of dye structure and hydrophilicity on the spectroscopic properties of IgG conjugates. Bioconjug. Chem. 22, 1298–1308 (2011).
pubmed: 21585199
doi: 10.1021/bc1004763
Nishio, N. et al. Optimal dosing strategy for fluorescence-guided surgery with panitumumab-IRDye800CW in head and neck cancer. Mol. Imaging Biol. 22, 156–164 (2020).
pubmed: 31054001
pmcid: 7017887
doi: 10.1007/s11307-019-01358-x
Wilson, R. H., Nadeau, K. P., Jaworski, F. B., Tromberg, B. J. & Durkin, A. J. Review of short-wave infrared spectroscopy and imaging methods for biological tissue characterization. J. Biomed. Opt. 20, 030901 (2015).
pubmed: 25803186
pmcid: 4370890
doi: 10.1117/1.JBO.20.3.030901
Cao, J. et al. Recent progress in NIR-II contrast agent for biological imaging. Front. Bioeng. Biotechnol. 7, 487 (2019).
pubmed: 32083067
doi: 10.3389/fbioe.2019.00487
Dreher, M. R. et al. Tumor vascular permeability, accumulation and penetration of macromolecular drug carriers. J. Natl Cancer Inst. 98, 335–344 (2006).
pubmed: 16507830
doi: 10.1093/jnci/djj070
Onda, N., Kimura, M., Yoshida, T. & Shibutani, M. Preferential tumor cellular uptake and retention of indocyanine green for in vivo tumor imaging. Int. J. Cancer 139, 673–682 (2016).
pubmed: 27006261
doi: 10.1002/ijc.30102
Newton, A. D. et al. Optimization of second window indocyanine green for intraoperative near-infrared imaging of thoracic malignancy. J. Am. Coll. Surg. 228, 188–197 (2019).
pubmed: 30471345
doi: 10.1016/j.jamcollsurg.2018.11.003
Ishizawa, T., Saiura, A. & Kokudo, N. Clinical application of indocyanine green-fluorescence imaging during hepatectomy. Hepatobiliary Surg. Nutr. 5, 322–328 (2016).
pubmed: 27500144
pmcid: 4960410
doi: 10.21037/hbsn.2015.10.01
Harris, J., Kajdacsy-Balla, A. & Chiu, B. Creation of a murine orthotopic hepatoma model with intra-abdominal metastasis. Gastroenterol. Hepatol. Bed Bench 9, 174–179 (2016).
pubmed: 27458509
pmcid: 4947131
Troyan, S. L. et al. The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping. Ann. Surg. Oncol. 16, 2943–2952 (2009).
pubmed: 19582506
pmcid: 2772055
doi: 10.1245/s10434-009-0594-2
Tian, R. et al. Multiplexed NIR-II probes for lymph node-invaded cancer detection and imaging-guided surgery. Adv. Mater. 32, e1907365 (2020).
pubmed: 32022975
doi: 10.1002/adma.201907365
Usama, S. M., Inagaki, F., Kobayashi, H. & Schnermann, M. J. Norcyanine-carbamates are versatile near-infrared fluorogenic probes. J. Am. Chem. Soc. 143, 5674–5679 (2021).
pubmed: 33844539
doi: 10.1021/jacs.1c02112
Hatami, S. et al. Absolute photoluminescence quantum yields of IR26 and IR-emissive Cd
pubmed: 25407424
doi: 10.1039/C4NR04608K
Würth, C., Grabolle, M., Pauli, J., Spieles, M. & Resch-Genger, U. Relative and absolute determination of fluorescence quantum yields of transparent samples. Nat. Protoc. 8, 1535–1550 (2013).
pubmed: 23868072
doi: 10.1038/nprot.2013.087
Nani, R. R. et al. In vivo activation of duocarmycin-antibody conjugates by near-infrared light. ACS Cent. Sci. 3, 329–337 (2017).
pubmed: 28470051
pmcid: 5408340
doi: 10.1021/acscentsci.7b00026
Institute for Laboratory Animal Research. Guide for the Care and Use of Laboratory Animals. 8th edn (National Academies Press, Washington, DC, 2011).