A novel mesoionic carbene based highly fluorescent Pd(II) complex as an endoplasmic reticulum tracker in live cells

Sanjay K. Verma a, Pratibha Kumari b, Shagufi Naz Ansari a, Mohd Ovais Ansari a, Dondinath Deori a and Shaikh M. Mobin *abc
aDiscipline of Chemistry, India. E-mail: xray@iiti.ac.in
bDiscipline of Biosciences and Biomedical Engineering, India
cDiscipline of Metallurgy Engineering and Materials Science, Indian Institute of Technology Indore, Simrol, Khandwa Road, Indore 453552, India

Received 6th July 2018 , Accepted 29th August 2018

First published on 30th August 2018

A recent study advocates that endoplasmic reticulum (ER) dysfunction may be linked to critical neurotrauma and advanced tauopathy. In this regard, targeting the ER warrants urgent attention towards the therapeutic treatment of neurotrauma-related neurodegeneration. Herein, we report the synthesis of a new N-heterocyclic mesoionic carbene based highly fluorescent square-planar Pd(II) complex 1, with a high quantum yield (0.737). Probe 1 is a non-toxic probe for selectively labeling the endoplasmic reticulum in live cells.

Owing to the advancement in bio-imaging techniques, the in vivo subcellular organelle targets and biochemical processes have gained much attention towards basic biomedical research and the development of novel clinical diagnostics.1–3 In this regard, some organic ligand and metal complex based probes have been explored.4–6 Among the sub-cellular organelles, the endoplasmic reticulum (ER) plays an important role in eukaryotic cells7 in the synthesis and processing of proteins, and calcium storage.8,9 Improper protein folding may interfere with ER functions. A recent development suggests that ER dysfunction is directly linked to many metabolic diseases, such as diabetes, obesity, insulin resistance, critical neurotrauma and advanced tauopathy.10–12

The design and synthesis of an appropriate chemical probe as the tool for the diagnosis and monitoring of diseases as well as biomarkers are the current area of focus. Understanding the complex molecular interactions in the human physiological system had posed a challenge to both chemists and biologists. Therefore, fluorescent probes have become popular because of their low cost, sensitive nature and ease of operation and use in bioactive molecules in living systems for both in vitro and in vivo studies. To understand the desired selectivity towards selective organelles, the recognition site of a fluorescent probe is designed in such a way that it maximizes the binding interactions.13–18 Furthermore, fluorescence recovery after photobleaching (FRAP) is widely used as a powerful tool for monitoring the molecular dynamics of fluorescent-tagged molecules within living cells by employing confocal microscopes (CSLMs).19

There exist few reports on ER tracking by employing some metal complexes,20 oxovanadium(IV) vitamin-B6 Schiff base complex,21 and tunicamycin-treated and organoplatinum(II) complexes containing bis(N-heterocyclic carbene)22 but all of these lack FRAP.

So far, reports on Pd complexes being engaged in anti-bacterial, anti-fungal, anti-viral and, more recently, anti-cancer activities with a focus on tumor cell lines like breast and prostate cancer by using different ligands such as triazole, dithiocarbamate,23 triphenylphosphines,24 hydrazine25 and even curcumin, which is a well-known plant-based compound with apoptosis-inducing activity on cancer cells, are well documented. Furthermore, better lipophilicity or solubility results in enhanced cytostatic activity of Pd(II) complexes. Only one report is available on Pt(II) complex based ER tracking, but to the best of our knowledge this is the first report on a MIC based Pd(II) complex as an efficient ER tracker.23–29

Herein, we report the synthesis of a phenylene based MIC ligand forming a Pd(II) complex and its biological evaluation which by large has been ignored to date.

Pd(II) complex 1 was synthesized by the Cu(I) catalyzed click reaction of 4-ethynyl toluene and sodium azide in the presence of sodium ascorbate and copper sulfate in a tert-butanol and water mixture; then the resulting product was converted into its triazolium iodide salt. This triazolium salt upon reaction with PdCl2 in the presence of a base resulted in the formation of complex 1 (Scheme 1). The Pd(II) complex 1 is highly soluble in dichloromethane and ethyl acetate. 1 was characterized by 1H, 13C NMR, FTIR and mass spectroscopy and further authenticated by single crystal X-ray studies. The FTIR spectroscopy of 1 reveals the band at ∼3100–3000 cm−1 which corresponds to the presence of aromatic (C–H) stretching vibrations.30 The 1H NMR spectrum does not show the triazolium signal after substitution with palladium. The 1H NMR spectra of 1 shows the absence of the azolium C–H proton which was observed at δ = 8.43 ppm in its parent 1-methyl-4-(p-tolyl)-1H-1,2,3-triazole compound. The resonance for the aryl C–H protons (δ = 7.37 ppm) is significantly downfield shifted compared to their corresponding resonance (δ = 7.21 ppm) in complex 1 (Fig. S1 and S3). The resonance for the C–H protons of the pyridine ring was detected as a multiplet at δ = 8.93, 7.78–7.80 and 7.66 ppm. Upon complex formation (1) the resonance for the α-hydrogen atom of the pyridine ring (δ = 8.93) was more downfield shifted compared to its corresponding resonance in free pyridine (δ = 8.62).31 The resonance for the characteristic carbene carbon atom was observed at δ = 137.1 ppm in the 13C NMR spectra of complex 1 which is quite similar to that of the corresponding compound (δ = 137.6 ppm).32 The resonance for the α-carbon atom of the pyridine ring appeared downfield shifted: δ = 154.5 ppm (Fig. S2 and S4), compared to its corresponding resonance in free pyridine. The LC-MS spectrum shows peak at 697.7 which corresponds to [M + 2Cl]+ (Fig. S5), suggest the formation of the Pd(II) complex 1.

image file: c8dt02778a-s1.tif
Scheme 1 Schematic representation of the synthesis of Pd(II) complex 1.

A single crystal suitable for X-ray diffraction study was obtained by slow evaporation of the dichloromethane–hexane solution of 1 at room temperature. Complex 1 that crystallizes in the monoclinic P21/n space group reveals the formation of the mononuclear 1 (Table S1). The Pd(II) atom in 1 is coordinated by a C-donor from the MIC ligand and a N-donor from pyridine, in a trans-fashion, and the remaining coordination sites are occupied by two iodide donors (Fig. 1a) forming a square planar geometry around the Pd atom. The C9–Pd1–N4 bond angle is almost linear at 177.77(5)° and the Pd1–C9 (1.967(8) Å) and Pd1–N4 (2.100(6) Å) bond lengths are in the range previously described for Pd(II) MIC complexes.33,34 The dihedral angle between the NHC plane {N1 N2 N3 C8 C9} and the phenyl ring plane {C2 C3 C4 C5 C6 C7} is found to be 43.09° (Fig. S6). The Pd–Py and triazole carbon–Pd moieties are twisted in the opposite direction, thus featuring the anti-geometry of the complex 1 (Fig. 1a).

image file: c8dt02778a-f1.tif
Fig. 1 (a) Perspective view of 1. (b) Helical view of 1via intermolecular I2⋯H4–C4 interactions.

The packing diagram of 1 reveals the presence of the C–H⋯I interaction. The intermolecular C(4)–H(4)⋯I(2) interactions, 3.092 Å, involve the donor carbon atom of the phenyl group and the acceptor I(2) atom of the other molecule leading to the formation of 1D polymeric chains (Fig. S7) resembling the single-stranded helical structure of 1via the I2⋯H4–C4 interaction along the b-axis (Fig. 1b and S8).

The electronic absorption and emission spectra of 1 were recorded in a tetrahydrofuran solution. The absorption bands of 1 at 233, 282 and 371 nm are attributed to the π → π* (aromatic moiety) and n → π* (triazole and pyridine) transitions respectively, for the ligand moiety, occurring due to the hetero-aromatic moiety (Fig. 2). The fluorescence emission data of 1 were obtained in a tetrahydrofuran solution upon excitation at λex = 371 nm. The emission spectrum of 1 exhibited the highest intensity band at 405 and 430 nm via vibronic splitting (Fig. 2). Moreover, the Stokes shifts of Pd(II) complex 1 were found to be 34 and 59 nm. The quantum yield of 1 was found to be very high, 0.737 (Fig. 2).

image file: c8dt02778a-f2.tif
Fig. 2 UV-visible (black) and fluorescence spectrum (blue) of the complex 1 at room temperature in 10−4 M tetrahydrofuran solution.

We recorded the emission spectra of Pd(II) complex 1 in 1% DMSO with various solvents (acetonitrile/THF/methanol/water) and found that the emission band splits into two partially resolved bands except in water (Fig. S9). This may be due to the strong hydrogen bonding between complex 1 and H2O which locks the molecule for vibronic coupling. The fluorescence intensity of 1 was found to be trivial quenching at high pH (phosphate buffer saline containing 1% DMSO at various pH values); this may be due to the formation of the electron donor 1,2,3-triazole/iodine, through photo-induced electron transfer (PET) under basic conditions. 1 showed a slight red shift with a decrease in pH up to 3.1 and was quite stable up to pH 7.4 (Fig. 3A). The fluorescence emission of 1 was also investigated in the micelles of positively charged cetyl-trimethyl-ammonium bromide (CTAB) and negatively charged sodium dodecyl sulfate (SDS) at 5.0 mM and 2.0 mM concentration respectively for mimicking the probe in the cell membranes (Fig. 3B and C). In addition, the fluorescence behaviors of 1 were unaffected at the studied pH range, indicating that the binding of the probe to the micelles efficiently shields the probe from the aqueous environment. These results imply that 1 can be localized in the membrane phases rather than in the aqueous phase in the cells.

image file: c8dt02778a-f3.tif
Fig. 3 (A) Fluorescence spectra of Pd(II) complex 1 (10 μM) in different pH solutions {1% DMSO in PBS (phosphate-buffered saline)} upon excitation at 371 nm. (B) In the presence of 5.0 mM CTAB (positively charged micelles). (C) In the presence of 2.0 mM SDS (negatively charged micelles).

The Pd(II) complexes are known for their extraordinary photoluminescence due to the σ-donating property of the anionic carbons, which effectively raises the energy of the d–d states, diminishing their deactivating effect.33,34 Furthermore, the photoluminescence spectra of 1 show two separate electronic transitions at 370 and 392 nm attributed to π* → π and π* → n transitions for the ligand moiety (Fig. S10) upon excitation at 25 °C (λex = 282 nm) as expected in such Pd(II)/Pt(II) complexes.35–37

The highly fluorescent nature of 1 prompted us to explore the role of 1 in live cells as a potential candidate for cellular organelle marker. To initiate biological activities, probe 1 was checked for cytotoxicity on both cancerous and normal cells, i.e. HeLa (cervical cancer cells) and HEK 293 (human embryonic kidney cells 293) cells, and was found to be non-toxic at a concentration up to 180 μM for 24 h as proved by the cell viability assay using MTT (Fig. S11). Furthermore, flow cytometry acquires superior quality fluorescence signals with an elevated spatial resolution from a significant population of cells in flow.38–40 Probe 1 labeled HeLa cells were estimated by flow cytometry (Fig. S12). The mean fluorescence intensity of a huge number of cells shifted from quadrant Q3–2 (control) to Q4–3 (treated) (Fig. S12a) and a subsequent shift in the histogram towards higher intensity was also observed (Fig. S12b). Moreover, the mean fluorescence intensity of the untreated cells was as low as 62 as compared to the treated cells having a higher mean fluorescence intensity of 2759. This indicates that 1 can uniformly label an enormous population of cells, which was detected in live cell suspensions by flow cytometry. The rapid population-based fluorescence statistical data of flow cytometry are further supported by the pictorial images obtained from confocal laser scanning microscopy.

To confirm the initial cellular location of probe 1, HeLa cells were treated with probe 1, and the images were captured in both blue and red channels. The probe is fluorescent in the blue channel and non-fluorescent in the red channel; hence probe 1 was excited by 405 nm not by 599 nm (Fig. S13). Therefore we performed co-localization experiments with three commercially available red fluorescent organelle trackers (ER-Tracker Red for the endoplasmic reticulum, MitoTracker Red CMXRos for mitochondria and LysoTracker Red DND99 for lysosomes). The fluorescent co-localization images (pink) of 1 with these organelle trackers (Fig. 4) indicated that 1 overlapped well with ER-Tracker Red with a high Pearson's co-localization coefficient Rr = 0.75 (Fig. 4a and 5). However, the poor colocalization effect were observed for mitochondria (Rr value = 0.44) and lysosomes (Rr value = 0.49) (Fig. 4b and c). Moreover, Manders’ coefficients were calculated with Manders’ M1 = 0.901 and Manders’ M2 = 0.679 signifying good colocalization of probe 1 (blue) and ER-Tracker Red (red) on a per-pixel level. This demonstrates that the probe 1 is highly selective towards localization in the endoplasmic reticulum and also compatible for counter-staining with LysoTracker Red and MitoTracker Red.

image file: c8dt02778a-f4.tif
Fig. 4 HeLa cells co-labeled with 1 (100 μM) and organelle markers. (a) ER-Tracker Red for the endoplasmic reticulum (1 μM); (b) MitoTracker Red CMXRos (80 nM) for mitochondria; (c) LysoTracker Red DND-99 (100 nM) for lysosomes. The images from left to right show probe 1 (column 1), organelle trackers (column 2), phase contrast (column 4), Overlay 1: overlay of the 1st and 2nd columns, and Overlay 2: overlay of the 1st, 2nd and 4th columns. Scale bar: 40 μm.

image file: c8dt02778a-f5.tif
Fig. 5 ER selective imaging of living HeLa cells treated with 1. Live HeLa cells treated with 1 (100 μM) and ER-Tracker Red (1 μM). The fluorescence emission of 1 (blue). The ER-Tracker Red (red) colocalization of these two fluorophores is overlay 1 and 2 (pink). Pearson's colocalization graph (yellow). Probe 1: λex = 405 nm, λem = 415–470 nm; ER-Tracker Red: λex = 559 nm, λem = 580–700 nm.

Photostability plays an important role for any marker in the cell to observe long-term imaging during physiological and morphological alterations within a stipulated time. In this regard, the photostability of 1 was studied in live HeLa cells and was compared with commercially available ER-Tracker Red. The fluorescence intensity initially decreases and after 200 scans it reaches 70% due to photobleaching but gradually recovers again up to 98% after 1800 scans (Fig. 6, Movies S1 and S2).

image file: c8dt02778a-f6.tif
Fig. 6 Comparisons of the photostability of probe 1 and ER-Tracker Red in HeLa cell lines. (a) Confocal images of 1 (100 μM, λex = 405 nm, λem = 415–470 nm) and ER-Tracker Red (1 μM, λex = 559 nm, λem = 580–700 nm) for photobleaching in HeLa cells. (b) Comparative photostability graph of ER-Tracker Red and 1.

This results in fluorescence recovery after photobleaching (FRAP) in the case of 1. This may be due to any of the following reasons: (i) diffusion of soluble fluorescent probe 1 in the ER membrane and (ii) the movement of 1 between organelles. In contrast, the ER-Tracker Red shows very poor photostability with the intensity being reduced to 20% of the initial intensity after 1800 scans, and could not recover during laser scanning.

3D tumor spheroids possess numerous features that mimic in vivo tumors such as cell–cell interaction, hypoxia cells at the center and a well-oxygenated outer layer of the cells. In order to explore 1 towards 3D tumor spheroids, the fluorescence images were captured every 2 μm along the Z-axis. 1 penetrates to a depth of ∼48 μm whereas the ER tracker penetrates up to ∼24 μm depth (Fig. S14, S15 and Movie S3, 4). This suggests that the compound 1 exhibited more fluorescence in the deep layer cells of spheroids as compared to the standard dye.


In conclusion, we report a rare example of the synthesis of new organometallic MIC based mononuclear Pd(II) complex 1. The higher quantum yield and non-toxic nature of 1 make it a potential candidate for inter-cellular uptake. The fluorescence behavior of 1 was unaffected at a broad pH range, indicating that the binding of the probe to the micelles efficiently shields the probe from the aqueous environment. Thus 1 specifically targets the ER of live cells and plays an important role in the movement of particles between organelles due to the fluorescence recovery after photobleaching (FRAP) property. 1 shows a rare FRAP property as compared to the so-far reported Pd/Pt complexes as well as commercially available ER-Tracker Red. All these properties make 1 a potential candidate for commercial use.

Conflicts of interest

There are no conflicts to declare.


The authors are grateful to the Sophisticated Instrumentation Centre (SIC), IIT Indore for providing characterization facilities. SKV is grateful to the SERB for providing National Post-Doctoral Fellowship; PK and SNA are thankful to the MHRD, New Delhi for fellowship; and MOA is thankful to IIT Indore for his internship. DND is thankful to IIT Indore. SMM is thankful to the SERB-DST (Project No. EMR/2016/001113), New Delhi, Government of India and IIT Indore for financial support. This work is dedicated to Professor Dr Dietmar Stalke on his 60th birthday.

Notes and references

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Electronic supplementary information (ESI) available. CCDC: 1573135. For ESI and crystallographic data in CIF or other electronic format see DOI: 10.1039/c8dt02778a
Crystal data of 1: C16H18I2N4Pd, M = 626.54, monoclinic P21/n, Z = 4, T = 293(2) K, F(000) = 1176.0, a = 10.7786(5) Å, b = 8.1520(3) Å, c = 23.4486(10) Å, α = 90°, β = 99.338(4)°, γ = 90°, V = 2033.06(15) Å3, size = 0.25 × 0.23 × 0.2, Index ranges = −14 ≤ h ≤ 13, −10 ≤ k ≤ 11, −29 ≤ l ≤ 31, Radiation = MoKα (λ = 0.71073), μ = 3.953 mm−1, 2Θ range for data collection = 6 to 57.682, GOF = 1.045, Reflections collected/Independent = 11[thin space (1/6-em)]043/4670 [Rint = 0.0283, Rsigma = 0.0267], R indexes [I ≥ 2σ (I)] = R1 = 0.0434, wR2 = 0.1117, R indexes [all data] = R1 = 0.0488, wR2 = 0.1154, CCDC 1573135.

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