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Excitation- and emission wavelength-based multiplex spectroscopy using red-absorbing near infrared-emitting lanthanide complexes Ruisheng Xiong, Dimitrije Mara, Jing Liu, Rik Van Deun, and Katalin Eszter Borbas J. Am. Chem. Soc., Just Accepted Manuscript • Publication Date (Web): 18 Aug 2018 Downloaded from http://pubs.acs.org on August 18, 2018
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Excitation- and emission wavelength-based multiplex spectroscopy using red-absorbing near infrared-emitting lanthanide complexes Ruisheng Xiong,† Dimitrije Mara,‡ Jing Liu,‡ Rik Van Deun,‡ K. Eszter Borbas†,* † Department of Chemistry, Ångström Laboratory, Uppsala University, Lägerhyddsvägen 1, 75120, Uppsala, Sweden 3 ‡ L – Luminescent Lanthanide Lab, Department of Chemistry, Ghent University, Krijgslaan 281, Building S3, B9000 Gent, Belgium Supporting Information Placeholder ABSTRACT: Multiplex imaging in the red and near infrared (NIR) should be an enabling tool for the real-time investigation of biological systems. Currently available emitters have short luminescent lifetimes, broad absorption and emission bands, and small Stokes shifts, which limits multiplexing in this region to two colors. NIR-emitting luminescent lanthanide (Ln) complexes carrying hydroporphyrin (chlorin) sensitizing antennae are excitable in the red through the narrow, intense and tunable chlorin absorptions. Both emission- and excitation-based multiplexing are possible, the former by exciting the same antenna appended to different Lns, the latter by attaching different chlorins with non-overlapping absorptions to the same Ln. The combination of excitation and emission spectroscopies allows for the straightforward differentiation of up to four different complexes.
1) light harvesting antennae, which allow for excitationwavelength-based discrimination in addition to emissionbased multiplexing. Up to 4 luminescent species could be readily identified.
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Multiplex fluorescence imaging offers information at a level of detail that is beyond the reach of single fluorophores. These tools are particularly valuable for studying complex systems e.g. in fundamental cell biology or in cancer diagnos1-7 tics. Small-molecule organic fluorophores and fluorescent proteins are of limited use in multiplexing due to the broadness of their absorption and emission bands, which results in spectral crosstalk and complicated data interpretation. Emitters based on luminescent lanthanide complexes [Ln(III)] overcome this limitation, and enable both wavelength8-10 11 based and lifetime-based multiplexing. The former is by virtue of the sharp and mostly non-overlapping, metalspecific Ln emission peaks. The latter technique is underpinned by the variety of excited state lifetimes found in Ln(III) complexes, which can cover over 6 orders of magni6,12 tude, from hundreds of ns to several ms. Higher-order multiplexing, i.e. the combination of temporal and spectral signal separation is also possible: a long-lived Tb donor and two cyanine acceptors placed at different distances have 13 enabled the differentiation of up to 4 targets. The Laporteforbidden Ln(III) luminescence can be sensitized using lightharvesting chromophores (‘antennae’). For biological applications the near infrared (NIR) emitting Lns, Yb(III) and Nd(III), are preferred to minimize tissue damage and maximize signal penetration. Here, we show that the multiplexing capacity of NIR Ln(III) can be greatly expanded by combining them with red-absorbing hydroporphyrin (chlorin, Figure
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homoleptic complexes: M = Pd, [Ln(Chl3 Pd)3]3M = 2H, [Ln(Chl3 FB)3]3heteroleptic complexes: Y = H, X = Chl3Pd, [Ln(dpa)2Chl3Pd]2-
homoleptic complexes: M = Pd, R = H, [Ln(Chl15Pd)3]3M = 2H, R = H, [Yb(Chl15FB)3]3heteroleptic complexes: Y = H, X = Chl15Pd, [Ln(dpa)2Chl15Pd]2Y = H, X = Chl15FB, [Ln(dpa)2Chl15FB]2-
Figure 1. a) Comparing the multiplexing abilities of organic fluorophores and of chlorin-Ln dyads. The Cy5/Cy7 absorptions and emissions cover the 500–800 nm range, and they substantially overlap. Two judiciously chosen chlorins combined with two different Lns enable the separate addressing
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of two distinct excitation and two distinct emission channels. b) Prepared Ln-chlorin-dyads. Chlorins have intense and narrow absorptions (Qy-bands) in the red. This is beneficial for the optical imaging of biological materials due to the non-destructiveness of such low-energy light, and the better transparency of biological structures at long wavelengths. The position and intensity of this band is tunable by peripheral substitution and macrocycle metalation. For the types of chlorins used here (Figure 1b) (Qy) ~ –1 –1 14,15 39500–90300 M ⋅cm are typical. We hypothesized that chlorin antennae would provide access to red-absorbing, NIR-emitting Ln complexes with non-overlapping excitation bands. While Yb complexes with chlorin antennae have been 16-18 reported, most were not amenable to Q-band excitation, and the lack of excitation spectra left the sensitization by the chlorin unproven. Recently, Zhang and co-workers have developed Yb emitters based on perfluorinated porpho19,20 lactones and azlactols. These elegant systems allowed for efficient red excitation. However, no Nd analogues were reported, and the Q-bands are also weaker and broader than 15 those in the chlorins, which would make positional tuning and excitation-based multiplexing challenging. To overcome the challenges encountered with previous chlorin-Ln dyads, we designed 3:1 homoleptic and 1:2:1 heterolep21 tic complexes based on a dipicolinic acid (dpa) framework (Figure 1). Free base and Pd chelate chlorins were appended to the 4-position of the dpa through either the 3- or the 15position of the chlorin to yield a series of antennae with a range of Q-band absorption maxima (vide infra). The short Ln-antenna distances should enable efficient energy transfer. 22 Quenching O-H, N-H and C-H oscillators are excluded from the first coordination sphere. The 3 antennae in the 3:1 complexes were expected to increase complex brightness. Chlorins were prepared using modifications of the Lindsey 23-25 synthesis (see Supporting information). Peripheral substituents were introduced by Pd-catalyzed cross-couplings 26,27 using the appropriate bromochlorin precursors. Ln complexation was performed by titrating a known amount of + 28 x 2LnCl3 or [Ln(dpa)2] (Ref ) with Chl M . The ligands were 1 13 fully characterized using H and C NMR analysis, HR-ESIMS and UV-Vis absorption and emission spectroscopy. The identities of the complexes were supported by luminescence emission and UV-Vis absorption spectroscopies (vide infra). The UV-Vis absorption spectra of the chlorins are shown in Figure 2a. Pd-chelates had ~50 nm blue-shifted Qy-bands compared to the analogous free base compounds. The differences in the Soret band positions were negligible. The Qyband absorptions of free base chlorins and Pd chelates were well separated. The influence of the dpa-substitution was smaller than that of the metalation. 15-linked antennae had blue-shifted Qy-bands (by ~13–21 nm) compared to 3-linked ones. These observations are in line with previous reports on the effect of metalation and aromatic peripheral substitu18,29 tion. Importantly, these antennae can be combined pairwise to enable selective excitation of one in the presence of 3 15 3 15 the other (e.g. Chl Pd or Chl Pd with Chl FB or Chl FB). Apart from spectral tuning, palladation also promotes intersystem crossing, thus facilitating triplet-mediated sensitization pathways.
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Figure 2. a) Chlorin absorption spectra in MeOH, [Chl ] = 0.5 mM. b) Ln excitation spectra of complexes carrying 15 Chl Pd antennae in THF/water. c) and d) Excitation spectra of Nd (c) and Yb (d) complexes carrying the same chlorin
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With these data in hand, we evaluated the potential of our complexes for excitation- and emission based multiplexing. A 15 mixture of Nd and Yb complexes that carried Chl Pd antennae were excited at the chlorin Q-band (λex = 590 nm), which afforded both Nd and Yb emissions (Figure 3a). We could distinguish two Yb complexes carrying two different anten15 15 nae (Chl FB and Chl Pd) due to the differences in their excitation spectra (Figure 3b). A combination of the Yb com15 plexes of the free base and the Pd-chelates of Chl had an excitation spectrum displaying two distinct, well-separated excitation peaks in the red. The peaks were located at the same wavelengths as those of the individual components (Figure 3b). These results show that both excitation- and emission-based differentiation is possible in mixtures of Ln complexes, and that chlorin metallation (palladation) provides a sufficiently large shift of the Q-band to enable interference-free excitation of either the free base or the Pd chlorin in the presence of the other.
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Chlorin excitation afforded Ln-centered emission in every Ln complex (Figures S18-S55), the Ln excitation spectra were similar to the antenna absorptions (Figures 2b, S1-S17), confirming that Ln emission was sensitized by the chlorins. Crucially, the Qy-bands were clearly visible in the excitation 3 spectra (at λmax = 600 nm for Chl Pd, λmax = 590 nm for 15 3 Chl Pd, λmax = 645 nm for Chl FB, and λmax = 637 nm for 15 Chl FB). This unambiguously establishes that these tunable red features are suitable for the sensitization of NIR Ln emission; λex > 650 nm were available for both Yb and Nd complexes. Notably, fluorescence microscopy usually relies on near UV or blue-light excitation. While two-photon excitation is possible with red/NIR light, it requires expensive instrumentation, and the development of new emitters can 30-32 be challenging. Excitation maxima were only dependent on the chlorin and not on the Ln (Figure 2b). The antennae in heteroleptic complexes seemed to be more efficient sensitizers than in the homoleptic ones, despite the latter complexes having 3 times as many antennae (Figures 2c and d). This may be due to interaction of the chlorins in the 3:1 com33 plexes quenching the antenna excited states. The excitation wavelengths used here are the most red-shifted ones reported to date, exceeding the previously most red-shifted excita19 tion wavelengths (600 nm) by > 50 nm. The sensitized Nd emission spectra showed two peaks in the observed region, 4 4 assigned to the F3/2→ IJ (J = 9/2, 11/2; 890, 1064 nm, respectively) transitions. The 890 nm band overlapped with an emissive contaminant (or an instrumental artefact), which was also observed in some of the Yb spectra. Therefore, we relied on the 1084 nm peak for detecting Nd and the 980 nm 2 2 peak for Yb. The latter corresponds to the F7/2→ F5/2 transition.
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antennae in different architectures. [Chl ] = 27 μM ([complex] = 9 μM), λem = 980 nm for Yb, and 1060 nm for Nd. The uncomplexed ligands are not soluble in aqueous mixtures, hence the choice of MeOH for recording the absorption spectra.
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Figure 3. Multiplex detection with a) emission-based (λex = 590 nm) and b) excitation-based discrimination (λem = 980 nm), [complex] = 9 μM for single lanthanide complex concentrations (blue and red lines), [complex] = 4.5 μM for each lanthanide complex in the mixture, [lanthanide] = 9 μM total (black line). Spectra were recorded in water/THF, the asterisk marks a peak that contains contributions from an artefact. These Ln complexes were substantially more photostable than a NIR-emitting cyanine dye currently used in microscopy (DTDCI, Figure 4). Photostabilities did not depend on the nature of the Ln ion. This is interesting, as a Nd-free base chlorin dyad could produce singlet oxygen through chlorin triplet excited state quenching by atmospheric oxygen; the triplet state was populated by thermal energy back transfer 17 from Nd. It is possible that singlet oxygen is not produced in our dyads, as the Pd chlorin triplet is higher-lying than that of the free base chlorin, which makes back energy trans18 fer unfavored. The Pd chlorin antenna without the Ln decomposed rapidly under the same conditions. Therefore, it seems that the Ln rapidly and irreversibly quenches the Pd chlorin excited state and prevents its reaction with atmospheric oxygen.
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Figure 4. Comparison of the photostabilities of a Nd and Yb 15 complexes of Chl Pd with a NIR-emitting cyanine dye, NTDCI (3,3’-diethylthiadicarbocyanine iodide, λex = 649 nm). λex = 390 nm for [Yb(Chl15Pd)3]3- and [Nd(Chl15Pd)3]3-. Water/THF were used as the solvent, and the absorptions of the solutions were adjusted to the same value. The connecting straight lines are there to guide the eye. Finally, we turned our attention to the sensitization mechanism to understand why the red-absorbing chlorins were competent antennae. Sensitization often proceeds via the 12 antenna triplet state. We studied the possibility of a singletmediated sensitization by comparing the residual chlorin 3 3 3 fluorescence in Nd(Chl FB)3, Yb(Chl FB)3, and Gd(Chl FB)3 (Figure S56,57). Gd(III) has only high-lying excited states, and thus cannot accept energy from the antenna. Compared to the Gd complex, the Nd and the Yb species had diminished chlorin fluorescence (Figure S57), which may be due to direct energy transfer from the chlorin singlet excited state. A photoredox mechanism involving electron transfer (eT) from the excited antenna to Yb(III), followed by back electron transfer to the antenna radical cation is known for Yb(III) complexes, and would also diminish the antenna 34,35 fluorescence. However, eT can explicitly be ruled out in the case of chlorin antennae by estimating the driving force 36 for eT. Typical 10-aryl-substituted chlorins have first oxidation potentials at ~1.03 V vs NHE. The Yb(II/III) redox poten37 tial for the hydrated ion is –1.15 V. This value is an upper estimate, as the overall 3– negative charge of the complex likely stabilizes Yb(III), and shifts the reduction to more negative potentials. The driving force for PeT from the excited singlet state of the chlorin (1.97 eV) is thus endergonic by 0.21 eV, so unfavorable (without the usually small contribution of the attraction between the Yb(II) and the chlorin radical cation). Therefore, we conclude that the efficient –1 overlap of the chlorin singlet (~15000–17000 cm ), and triplet –1 38 (~13000 cm for an analogous 15-Ph Pd chlorin) excited –1 3+ states, which are located < 5000 cm above the Nd (11200 –1 3+ –1 cm ) and Yb excited states (10300 cm ), are the most likely sources of Ln sensitization (Figure 5).
Figure 5. Proposed sensitization pathway with contributions from the chlorin singlet and/or triplet excited states (left), and the unlikely Yb sensitization based on stepwise electron transfer (right). In conclusion, a series of chlorin-Ln dyads have been prepared and characterized. Complex synthesis proceeds through a number of robust, high-yielding steps. Both free base and Pd chlorins were competent antennae for Yb and Nd, enabling Ln luminescence sensitization with red light; excitation at wavelengths exceeding 600 nm were possible. The combination of narrow Ln emissions with narrow chlorin absorptions provides avenues for excitation and emissionbased multiplex imaging. The straightforward tuning of the chlorin absorptions greatly increases the number of potentially detectable species in complex mixtures using benign red excitation and NIR emission.
ASSOCIATED CONTENT Supporting Information Synthetic procedures, characterization data for all new compounds, additional photophysical characterization, previously reported chlorin-Ln dyads. This material is available free of charge via the Internet at http://pubs.acs.org.
AUTHOR INFORMATION Corresponding Author
[email protected] Notes The authors declare no competing financial interests.
ACKNOWLEDGMENT This work was supported by the Swedish Research Council (project grant 2013-4655 for K.E.B.). J.L. acknowledges the China Scholarship Council (CSC) for a doctoral grant (201507565008). D.M. thanks the Ghent University Special Research Fund (BOF) for a PhD position (BOF15/24J/049). We thank Dr. Julien Andrès for critically reading the manuscript and for pertinent discussions.
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