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Metal Complexes in Application of Two-Photon Luminescence Probes

Jiaen Xie , Yuheng Luo , Qianling Zhang , Pingyu Zhang

Progress in Chemistry ›› 2021, Vol. 33 ›› Issue (1) : 111 -123.

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Progress in Chemistry ›› 2021, Vol. 33 ›› Issue (1) : 111-123 DOI: 10.7536/PC200557
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Metal Complexes in Application of Two-Photon Luminescence Probes
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Abstract

During the past years, metal complexes have attracted intensive research interest in biological sensors and imaging of cellular dynamics during a series of biological events. This is due to their unique advantages includes the following:(1) easily tunable chemical and photophysical properties resulting from their synthetic versatility;(2) high emission quantum yields and long phosphorescence lifetimes, which may avoid interferences from background auto-fluorescence;(3) large Stokes shifts for effective discrimination of excitation and emission wavelengths, as well as prevention of fluorescence quenching induced by self-absorption, and(4) emissive properties that are sensitive to subtle changes in the local environment. In recent years, metal complexes with obvious two-photon absorption have been attracted extensive attention in luminescence detection of biomolecules and organelle dyes because of their superior depth resolution and low light damage compared with traditional one-photon absorption. This review describes the latest two-photon absorption metal complexes with detection of biomolecules(pH, O2, HClO, NO, SO2, GSH, DNA, and so on) for diagnosis of diseases, as well as organelle probes(mitochondria, lysosomes, lipid droplets, nucleus, and so on) for intracellular dynamic behaviors and evolution processes. Finally, the perspectives of metal complexes in application of biomolecular probes and organelle dyes were analyzed and discussed.

Contents

1 Introduction

2 Two-photon technology

2.1 Two-photon absorption

2.2 two-photon emission and Two-photon absorption parameters measurement

2.3 Study on two-photon luminescent probes of metal complexes

3 Two-photon luminescent biosensors

3.1 O2

3.2 Amino acids

3.3 DNA

3.4 pH

3.5 SO2

3.6 HClO

3.7 NO

3.8 Metal ions

4 Two-photon luminescent organelle dyes

4.1 Mitochondria

4.2 Lysosomes

4.3 Lipid droplets

4.4 Nucleus

5 Conclusion and outlook

Graphical abstract

Keywords

metal complexes / two-photon absorption / biosensors / organelle dyes

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Jiaen Xie, Yuheng Luo, Qianling Zhang, Pingyu Zhang. Metal Complexes in Application of Two-Photon Luminescence Probes. Progress in Chemistry, 2021, 33(1): 111-123 DOI:10.7536/PC200557

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1 Introduction

Two-photon technology is a new type of photon technology based on the theory of two-photon excitation. In the past decades, two-photon absorption (TPA) has attracted considerable interest due to its potential applications in fluorescence microscopy, photodynamic therapy (PDT), three-dimensional optical information storage, optical limiting, laser up-conversion and three-dimensional microfabrication[1 ⇓ ⇓ ⇓ ⇓~6][7 ⇓ ⇓~10][11 ⇓ ⇓~14][15 ⇓~17][18,19]. Among them, since the two-photon fluorescence microscopy (TPM) was proposed, many researchers have carried out a wide range of biological imaging studies[20]. Today, two-photon fluorescence microscopy has become an important research tool in chemical biology and biomedicine, and provides a visualization method for understanding life. TPM is often applied to the detection of biomolecules in living cells and the dynamic imaging of biological tissues, such as the dynamic behavior tracing of subcellular organelles (mitochondria, lysosomes, vacuoles, etc.), the visualization of drug release, the imaging of cancer cells and neural tissues, and the detection of disease-related biomolecules[21 ⇓ ⇓ ⇓ ⇓ ⇓ ⇓ ⇓ ⇓ ⇓~31].
Compared with the traditional single-photon excitation emission materials, two-photon excitation emission materials have been more widely used, which have the advantages of strong depth resolution and less optical damage. Moreover, most of these applications rely on two-photon fluorescence probes with strong two-photon absorption or excellent two-photon excitation emission (TPE). Therefore, the demand for the design and synthesis of efficient two-photon fluorescence probes is increasingly urgent. There have been comprehensive reviews in this area, however, these reviews have focused only on organic compounds[32 ⇓~34]. Compared with organic compounds, metal complexes have more advantages, such as versatile synthesis, tunable optical properties, high fluorescence quantum yield, long fluorescence lifetime, large Stokes shift and so on[35 ⇓ ⇓ ⇓~39]. In recent years, metal complexes have been widely studied as two-photon fluorescence probes in ions, gas molecules, biomolecules, organelle dyes and so on, opening up a new field of biomedicine. In this context, this review focuses on the recent progress in the application of metal complexes in two-photon fluorescence sensing of biomolecules and dye tracing of cellular organelles.

2 Two-photon technique

2.1 Two-photon absorption

Normally, for an electron to jump from a lower energy level to a higher energy level, it must absorb an energy equivalent to the difference between the two energy levels. If this energy is provided by light radiation, it will only be absorbed by atoms when the energy of the photon is the difference between the two energy levels. Although the energy of one photon is less than the difference between two energy levels, electrons can absorb two photons at the same time to reach a certain energy and complete a transition, which is called two-photon absorption (TPA)[40]. The theory of TPA was first proposed by Maria Goeppert-Mayer, a Nobel laureate in physics, in 1963, but Kaiser and Garret first demonstrated the TPA process in 1961[32][34]. Two-photon absorption mainly occurs at the focus of the ultra-intense laser generated by the pulse laser, and the laser intensity at other places on the optical path is not enough to produce two-photon absorption, while the corresponding single-photon process can not occur due to the longer wavelength and lower energy of the light used, so the two-photon process has good spatial selectivity and less damage to the sample.

2.2 Two-Photon Emission and a Parameter for Measuring Two-Photon Absorption Capability

The molecule absorbs energy from a single photon and radiates back to the ground state from the electronic excited state, which is called single photon emission (OPE). In most cases, the emitted light has a longer wavelength and is therefore lower in energy than the absorbed radiation (Stokes shift). The two-photon emission (TPE) process is similar to the single-photon emission described above, but the main difference is that the energy required for the transition of an electron in a molecule from a ground state to an excited state and back to the ground state is excited by two photons, each of which contributes half of the total energy required to induce emission. Therefore, the emission light has a shorter wavelength than the excitation light (fig. 1).
The TPA cross section (δ) is an important parameter reflecting the TPA ability of molecules in the TPA phenomenon, and two-photon excitation emission (TPE) is one of the main techniques to measure it[35]. According to this theory, Lambert-Beer derived the equation (Equation 1) for calculating the TPA cross section (δ):
δ = hν N 0 = 10 3 hνβ N A C
The unit of δ is Goeppert-Mayer(GM),N0 is the number density of absorption centers, NA is Avogadro's constant, C is the molar concentration of the solute, and β is the value of the two-photon absorption coefficient (determined by fitting the experimental results with a self-compiled program)[35].
The TPA cross section (δ) plus the fluorescence quantum yield () is the two-photon absorption cross section, another parameter commonly used to describe TPA molecules. Since light stability is one of the important criteria for the development of fluorescent imaging agents, Belfield et al. defined a new value (FM) to estimate the potential of TPA fluorescent probes (Equation 2):[33,36][37]
F M = δ Ф f Ф d
Is the TPA cross section, the Фf is the fluorescence quantum yield, and the Фd is the photolysis quantum yield[33]. The introduction of the Фd of photolysis quantum yield in the FM provides a more accurate method for the determination and comparison of the potentials of TPA fluorescence probes.

2.3 Study on Metal Complexes as Two-Photon Fluorescence Probe

In 2008, Williams et al. First used two-photon technology to apply metal complexes to biological imaging dyes. Compared with organic compounds, metal complexes have attracted much attention because of their unique advantages in biological imaging and therapy.Comprises the following steps: (1) the metal complex is formed by complexing a plurality of components, and a series of analogues with different functional groups can be conveniently synthesized by changing one of the components, so that the photochemical or photophysical properties of the metal complex can be fine-tuned[38][39 ⇓~41]; (2) They have high luminescence quantum yield and long phosphorescence lifetime, and can effectively work under high fluorescence background by using time-resolved emission spectra to avoid the interference of background autofluorescence; (3) better photostability and water solubility, thus having larger Stokes shift, effectively distinguishing excitation wavelength from emission wavelength, and preventing fluorescence quenching caused by self-absorption; (4) Their photophysical properties are very sensitive to structural or environmental changes. Therefore, metal complexes have great potential as two-photon fluorescence probes to monitor various indices in cells.

3 Biomolecule two-photon fluorescence sensor

3.1 Oxygen

Molecular oxygen, which plays an important role in many physiological processes, has a significant impact on cell and tissue functions, including ATP and ROS production, signal transduction processes, ion flux, and enzyme conversion[43 ⇓~45]. Studies have found that circulatory hypoxia, that is, hypoxia followed by reoxygenation, can lead to the upregulation of HIF-1 activity in tumor cells and reduce the success rate of radiotherapy or chemotherapy. Therefore, it is of great significance to visually monitor circulatory hypoxia in cells and in vivo. Zhang and Chao et al. designed a series of ruthenium (II) anthraquinone complexes (1A ~ C) as two-photon fluorescence probes for the hypoxia-normoxia reversible process (Fig. 2). They first used rat liver microsomes (0.25 mg/mL) for extracellular experiments.The results showed that NADPH could catalyze the reduction of quinone derivatives in the presence of 50 μM NADPH as a cofactor, and the fluorescence intensity of these probes was significantly enhanced (more than 80 times) in the absence of oxygen, while there was no significant change in the fluorescence in the presence of oxygen[46]. Two-photon fluorescence confocal microscopy was used to monitor the two-dimensional and three-dimensional cellular hypoxia environment, and the probes 1a-c were applied to two-photon fluorescence imaging to detect the dynamic process of the reversible hypoxia-normoxia cycle in living zebrafish.
Then, they designed and synthesized a series of two-photon phosphorescent iridium (III) -anthraquinone complexes 2a ~ d (Figure 3), which were used for the detection of mitochondria in normoxic and hypoxic environments. Under hypoxic conditions, the reductase reduced the probe to hydroquinone derivatives. Under single-photon (λ = 405 nm) and two-photon (λ = 720 nm) excitation, the fluorescence intensity was significantly enhanced, and the two-photon absorption cross section at λ = 720 nm was 76 ~ 153 GM[47]. At the same time, the iridium (III) complex has high sensitivity and specificity, and can image and track the morphological changes of mitochondria in a long-term hypoxic environment.

3.2 Amino acid

Thiol amino acids (R-SH) play an important role in maintaining biological homeostasis, and their levels change significantly in response to oxidative stress, which is associated with toxic injury, bacterial infection, and disease[48 ⇓ ⇓ ⇓~52]. For example, cysteine (Cys) deficiency can lead to a variety of abnormalities, such as decreased hematopoietic function, leukopenia, psoriasis and so on. Hyperhomocysteinemia (Hcy) is a risk factor for cardiovascular and Alzheimer's disease. Glutathione (GSH) is involved in many important functions of the body, including the control of the intracellular redox environment[53 ⇓ ⇓~56]. Therefore, it is very important to develop biological probes that can detect thiol levels in vivo and in vitro. Zhang and Chao et al. designed and synthesized a two-photon ruthenium complex 3 (Figure 4), and combined it with gold nanoparticles to form a composite RuNH2@AuNPS, which is sensitive to biological thiol molecules, can specifically identify biological thiol in the presence of other amino acids and metal ions, and has good selectivity, fast reaction speed and low toxicity.When the thiol in living cells and living tissues is detected, the detection depth can reach 80 to 170 mu m, the two-photon fluorescence intensity and the two-photon absorption cross section are large at the same time, and the method is successfully used for detecting biological thiol in mouse hippocampus tissues and provides a good method for detecting biological thiol molecules in vitro and in vivo[57].
Tian et al. designed and synthesized two new cyclometalated iridium (III) complexes 4A and B with different electron donors (Figure 5). In the presence of Cys/Hcy, the synthesized cyclometalated iridium (III) complexes showed obvious fluorescence off-on reaction, and the response sensitivity of complex 4B to Cys/Hcy in vivo or in vitro was higher than that of complex 4A.And that probe can be effectively enrich in the mitochondria, thereby providing a two-photon fluorescence detection method for the content level of the mitochondrial Cys/Hcy in a living biological system[58].
In recent years, both monovalent and trivalent gold have been shown to react with proteins or enzymes containing cysteine or selenocysteine, which can be toxic to cisplatin-resistant cancer cells. Zou et al.These complexes are highly stable to thiol molecules in the dark, and can effectively dissociate hydrogen ligands to produce H2 under 365 nm light excitation, and react with sulfhydryl molecules (such as glutathione GSH, N-acetylcysteine NAC) to form Au-S reaction products[59 ⇓ ⇓ ⇓ ⇓ ⇓ ⇓ ⇓ ⇓~68][69]. Cell experiment show that that gold complexes can well inhibit the activity of TrxR unde the condition of illumination. And in zebrafish embryo experiment, that gold complex is proved to be capable of inhibit the thiol-containing enzyme, thereby leading to anti-angiogenesis activity. Meanwhile, these complexes can be activated by long-wavelength two-photon irradiation.Two-photon fluorescence microscopy analysis showed that 690-700 nm laser could effectively excite the fluorescence of 5 B in the cytoplasm of cancer cells, and the imaging was similar to that of 405 nm single-photon excitation.
Histidine (His) plays a vital role in maintaining healthy tissues and protecting nerve cells. In living cells, histidine, as a structural protein, is closely related to DNA and may lead to various diseases, such as asthma and advanced cirrhosis[70]. Therefore, it is necessary to develop a high quality histidine detection method. Tian et al. designed and synthesized a series of two-photon absorbing cyclometallic iridium (III) complexes, including complex 6 (fig. 7), which increases the solubility of the complex through the introduction of carboxylic acid groups and provides good biocompatibility[71]. The carboxylic acid group can accelerate the permeation of the iridium complex through the nuclear membrane, and the pyridine ring provides a lone pair electron to form a hydrogen bond with histidine, thereby stabilizing the molecule and increasing the water solubility in vivo and in vitro. In the near infrared region, complex 6 reacts with histidine/histidine-containing proteins to form luminescent products in the nuclear region of living cancer cells through secondary bond interactions. The two-photon absorption cross section can reach 40 GM. The results of two-photon confocal imaging showed that complex 6 could rapidly and selectively illuminate the nuclei of fixed and living cells under 820 nm excitation, and the distribution of histidine in the nuclei could be displayed in super-detail by using super-resolution (SR) technique under stimulated emission depletion microscopy (STED).

3.3 DNA

DNA is the carrier of genetic information in most organisms, so it is very important to detect the behavior and distribution of DNA in living tissues for the diagnosis of diseases[72 ⇓~74]. Designing probes that specifically bind to DNA and exhibit high fluorescence quantum yield after binding is of great importance for both research and clinical trials.
Thomas et al. designed and synthesized a pair of DNA-targeted ruthenium (II) complexes 7 a, B (Fig. 8), and used TP-PLIM imaging probe to detect nuclear DNA in living cells and fixed cells. The phosphorescence emission lifetime of the probe after binding with DNA was more than 160 ns, which was several orders of magnitude longer than the general phosphorescence emission lifetime imaging[75]. At the same time, complexes 7 a and B have different phosphorescence emission lifetimes between nucleus and cytoplasm, which will help to study the chromatin microenvironment in a variety of physiological environments, including proliferation, quiescence, senescence and cell cycle progression. This study provides a new method for the detection of DNA using two-photon phosphorescence lifetime imaging.
Tian et al. designed a cuprous cluster two-photon fluorescence probe 8 to observe DNA in the nucleus of MCF-7 cells (Fig. 8). The two-photon absorption cross section of the molecule in the near-infrared region (780.5 nm) is as high as 2850 GM.In addition, complex 8 has long fluorescence lifetime, high quantum yield and photostability, low cytotoxicity, and excellent two-photon fluorescence imaging performance, which make it an ideal two-photon DNA fluorescence probe[76].

3.4 pH value

Small changes in pH may lead to cell dysfunction, so the development of sensors that can easily monitor small changes in intracellular pH is essential to understand the relevant physiology[77 ⇓~79]. Chao et al. designed two pH-sensitive, two-photon absorbing morpholine-iridium complexes 9a, B (fig. 9), whose emission intensity increases linearly with increasing pH (in the range of 6.0 to 8.0), capable of tracking mitochondrial pH fluctuations during apoptosis[80].

3.5 SO2

Sulfur dioxide, sulfite, bisulfite and other substances are widely present in industry as air pollutants and are widely used as food preservatives[81]. However, abnormal levels of SO2 derivatives in the human body may cause allergic symptoms, such as dermatitis, diarrhea and asthma reactions. Serum total sulfite remained at a low level in healthy subjects[82 ⇓ ⇓~85]. However, the role of SO2 is still unclear, and a rapid, simple, non-invasive and reliable real-time detection method is needed. Chao et al synthesized and designed a series of two-photon phosphorescence probes to detect the distribution of SO2 derivatives in subcellular organelles[86]. Among the four iridium (III) complexes they synthesized, complex 10 (fig. 10) has the largest quantum yield and TPA cross section, and reacts rapidly to biological sulfite/bisulfite. Subsequently, two-photon excitation real-time imaging was used to observe in situ sulfite production in C. elegans and to monitor sulfite distribution in rat brain and other tissues. Thus, complex 10 can be used for two-photon fluorescence detection for direct visualization of SO2 derivatives in vivo.

3.6 HClO

Hypochlorous acid (HClO) is a reactive oxygen species that can be partially dissociated into hypochlorite ions at physiological pH. Endogenous hypochlorite is produced by enzymatic catalysis and has strong antibacterial properties[87,88]. However, excess hypochlorite can trigger a variety of diseases, including neuronal degeneration, cardiovascular disease, and osteoarthritis[89]. Therefore, the development of a HClO sensitive sensor suitable for life systems has become a hot topic. Chao et al. developed a two-photon fluorescence probe 11 (fig. 11) for the detection of HClO. The probe carries a diaminomaleonitrile group as a reactive moiety with the ClO-, which can selectively react with the ClO- to form an oxidized carboxylic acid product that exhibits a significant two-photon absorption cross section of 78.1 GM at 750 nm[90]. Meanwhile, the specificity of the two-photon fluorescence probe to the ClO- is higher than that of other ions and ROS, and the two-photon excitation detection is obviously superior to the single-photon excitation detection through experimental verification.

3.7 NO

Nitric oxide (NO), a ubiquitous cellular signaling molecule in the cardiovascular, immune, and nervous systems, plays an important role in human physiology and pathology. It has complex effects on the catabolic autophagy process and is closely related to lysosomal function[91 ⇓ ⇓~94]. Therefore, there is an urgent need to develop optical probes that can detect nitric oxide in lysosomes rapidly and selectively. Chao et al. designed and synthesized a two-photon phosphorescent iridium complex probe 12 for nitric oxide detection that targets lysosomes and is independent of pH (fig. 12)[95]. The probe can be used for biological imaging of two-photon phosphorescence intensity and phosphorescence lifetime. When the ratio of complex 12 to NO is 1 ∶ 0.2, the fluorescence lifetime is 280.2 ns, and when the ratio is 1 ∶ 1, the fluorescence lifetime increases to 617.3 ns. After incubation with complex 12, the changing levels of NO in macrophages and zebrafish were monitored by two-photon fluorescence imaging and fluorescence lifetime imaging, and these linearly changing fluorescence lifetimes also made them potential for quantitative analysis.
Ghosh et al. designed a copper complex (13) as a two-photon fluorescence probe for NO (fig. 13) and observed NO production by two-photon laser scanning microscopy (TPLSM)[96]. Complex 13 shows high sensitivity and specificity for NO and has low cytotoxicity. Which qualitatively and semi-quantitatively detects the production of endogenous NO. Next, the probe was shown to be useful for imaging NO production in endothelial cells and smooth muscle cells by observing ex vivo mounted rat carotid arteries and aortas via TPLSM. Specific visualization of nitric oxide production in blood vessels using complex 13 provides an effective method for studying the complex interaction between nitric oxide and vascular function.

3.8 Metal Ions

Metals in the form of ions can form biological complexes such as metalloproteins and metalloenzymes with biological ligands such as proteins, nucleic acids, vitamins, hormones and metabolites, and then play an important biochemical and physiological role in life processes. The level of metal ions in organisms is of vital importance and is increasingly becoming a standard for the diagnosis of diseases. They have played an increasingly important role in the extensive study and management of metabolic disorders and various diseases[97].
Copper is the third most abundant essential trace element in the human body and plays an important role in many basic physiological processes. The disruption of copper homeostasis may lead to neurodegenerative diseases, gastrointestinal disorders and liver and kidney damage[98 ⇓~100]. Fluorescent molecular probes have been proved to be a feasible method for the detection of Cu2+ because of their high sensitivity and simplicity[101]. Two-photon microscopy (TPM) uses two low-energy photons to obtain the excited state of the fluorophore, so it has the advantages of lower phototoxicity, better three-dimensional spatial localization, deeper penetration depth and lower self-absorption compared with single-photon absorption[32,102]. Chao et al. designed a novel binuclear Ru polypyridine complex 14 (fig. 14), which is a highly selective Cu2+ ion luminescence sensor with a low detection limit.Can be used in the presence of other abundant cellular cations such as Na+, K+,Mg2+, Ca2+, Zn2+ and Ag+),Because of its high two-photon absorption cross section up to 400 GM, good water solubility and membrane permeability, and low toxicity, it can be used as a sensor probe to detect Cu2+ in living cells and zebrafish[103].
Mercury is a highly toxic element, which can damage DNA, mitosis, central nervous system and endocrine system, and its detection methods have been widely studied in the field of sensing[104 ⇓ ⇓ ⇓ ⇓~109]. Fluorescent probes have become one of the important means of Hg2+ detection due to their advantages of high efficiency, sensitivity, rapid and convenient detection[110]. In combination with the nonlinear absorption and two-photon induced luminescence properties of the platinum (II) complex system, Kim et al. designed and synthesized a water-soluble rhodamine-platinum (II) complex 15 (fig. 15). After combining with the Hg2+, it was observed that the fluorescence of the complex 15 was enhanced by 20 times[106,107,111,112][113]. Therefore, the location of Hg2+ accumulation in cells can be observed by two-photon microscopy, and the trace mercury ions in living HeLa cells can be detected qualitatively, which is very helpful for scientists to study the role of Hg2+ in biological systems.

4 Organelle targeted two-photon fluorescent dy

4.1 Mitochondria

Mitochondria are energy factories and key regulators of cell death signals[114]. Through structural adjustment and molecular design, metal complexes can be located in specific organelles to achieve biological imaging applications at the subcellular level[115]. Intracellular viscosity, which affects protein-protein interactions on cell membranes, has been implicated in many diseases, such as atherosclerosis, diabetes, and Alzheimer's disease. In addition, the viscosity of the mitochondrial matrix is closely related to mitochondrial network organization, mitochondrial respiration, metabolite diffusion, and mitochondrial metabolism.
Mao et al. introduced a viscosity-responsive group into luminescent iridium complexes 16 a-f (fig. 16) that can aggregate in mitochondria. These iridium complexes respond specifically to the viscosity of mitochondria and have strong two-photon absorption and long fluorescence lifetimes (up to 1 ms)[116]. First of all, they confirmed that the reason why the emission intensity and lifetime of the complex are related to viscosity is mainly caused by the change of the configuration of the diphosphine ligand. Among them, 16 f could induce mitochondrial dysfunction, and the dynamic changes of mitochondrial viscosity in A549 cells treated with 16 f were tracked in real time by TPPLIM, which showed high TPA performance and good viscosity sensitivity. Therefore, complex 16 can provide a more accurate method for the quantitative detection of mitochondrial heterogeneity by TPPLIM.
Mitochondrial division and fusion is an important biological network dynamic process in cells[117 ⇓ ⇓ ⇓ ⇓~122]. In order to track the dynamic process of mitochondria, Chao et al. synthesized a series of cyclometallic iridium (III) complexes 17 a ~ e (Fig. 17) and proved that they can be used as two-photon fluorescent dyes for real-time imaging and tracking of mitochondrial fusion and division, providing a theoretical basis for the development of two-photon fluorescent dyes for mitochondria[123].

4.2 Lysosome

Lysosomes, like the stomachs of cells, degrade biological macromolecules through phagocytosis, autophagy and endocytosis, and play a key role in metabolism, cell antigen processing, cell migration, intracellular transport, plasma membrane repair, apoptosis and exosome release[124,125][126 ⇓~128]. The ability to track lysosomes over time is important for understanding the details of lysosomal function and for evaluating drug and gene delivery systems[129,130].
Chao et al. designed and synthesized a water-soluble iridium (III) tricyclic complex 18 (Fig. 18) linked with morpholine group. The phosphorescence intensity of 18 has a specific response to pH value and decreases with the increase of pH value, but no quenching occurs at high pH value[131]. The complex has strong two-photon absorption at 750 nm and can be used to stain lysosomes in living cells and three-dimensional tumor spheres. In addition, the morpholine group is protonated in the lysosome, and the complex 18 can label the lysosome for more than 4 days, so that the complex 18 can be used as a long-term probe and is expected to trace the process of the transfer and action mechanism of lysosomes in cells.
Subsequently, Stang and Chao et al. Obtained ruthenium-platinum metal compounds 19 a, B (fig. 19) with strong two-photon absorption by coordinating and assembling a ruthenium complex and a platinum complex[132]. The ruthenium and platinum metal compounds are encapsulated by liposomes to form nanoparticles, which accumulate in lysosomes after entering cells. The results show that the metal has deep red luminescence, large two-photon absorption cross section and high efficiency of ROS generation under illumination.

4.3 Lipid droplet

Lipid droplets (LDs) have become a hot topic in recent years because of their close relationship with lipid metabolism and many diseases[133,134]. Mao et al. designed two kinds of lipophilic neutral phosphorescent iridium (Ⅲ) complexes 20 a, B (Fig. 20 A). Both complexes 20 showed long-lived red phosphorescence with large Stokes shift (about 150 nm) and large TPA cross section (the TPA value of 20 a was 232 GM and the TPA value of 20 B was 220 GM). Complex 20 a was selectively accumulated in lipid droplets in cells, with high specificity, good biocompatibility and photostability[135]. Through the TPLIM and two-photon CLSM images of A549 cells labeled with complex 20 a, it was found that the hydrophobic and hypoxic environment of lipid droplets in cells increased the phosphorescence lifetime of complex 20 a, and then the distribution of lipid droplets in living cells was analyzed. Therefore, complex 20A is expected to be a probe for lipid droplet tracer analysis and has great potential to be used to visualize lipid metabolism in vivo.
Koshel et al. designed and synthesized a lipophilic phosphorescent gold (I) cluster complex 21 (Fig. 20B), which is selectively located in lipid droplets of adipocytes and other cells and has high two-photon absorption cross section and emission intensity[136]. The complex has a microsecond fluorescence lifetime in both solution and biological tissues, and is highly selectively localized and stained in lipid droplets of various adipose tissues (subcutaneous adipose tissue, visceral adipose tissue, and mesenteric adipose tissue) of different animals (pigeons, chickens, and mice) and in lipid droplets of HepG2 cells.

4.4 Nucleus

nucleus is the largest and most important cellular structure in eukaryotic cells, and its functions include gene expression, cell migration, homeostasis and other important physiological processes. It is of great significance to effectively monitor and image the biological properties of nucleus[137]. Tian et al. Synthesized four Zn (II) complexes 22a-d (Fig. 21a) based on two polypyridyl chromophoric ligands containing carbazole groups, and demonstrated experimentally and theoretically that the two different conjugated bridges (π and) of the tripyridyl ligands can cause different optical properties to a great extent, in which 22A enters cells through endocytosis and illuminates the plasma membrane and nucleus of living cells[138]. Efficiently diffuses in the cerebral chambers of juvenile and adult zebrafish and penetrates to depths in excess of 300 μm. In a mouse model, intravenous administration of 22 a showed high affinity with the blood-brain barrier and good penetration into brain parenchymal cells.
Next, Tian et al. Synthesized and characterized two new two-photon absorption organotin (IV) complexes 23 a and B (Fig. 21B). Compared with 23 a, the two-photon absorption cross section of 23 B in the near-infrared region was significantly enhanced. Through two-photon fluorescence microscopy imaging, it was found that 23 B could specifically target the nuclear DNA[139]. The mechanism shows that there are abundant hydrogen bonding interactions between the hydroxyl group of 23b and DNA. Carboxylate units can accelerate the penetration of organotin (IV) derivatives on cell membranes, while aniline groups with good planarity can be linked to DNA. In addition to targeting the nucleus, 23b has also been successfully applied as a two-photon anticancer agent to inhibit tumor growth.

5 Conclusion and prospect

Due to the remarkable advantages of two-photon laser and fluorescence microscopy in tissue imaging and disease diagnosis, many two-photon fluorescence probes have been studied recently. This review mainly summarizes the important applications of metal complexes in two-photon fluorescence probes of biomolecules and organelle dyes, and explains the application of metal complexes in two-photon detection of different biomolecules and the process of localizing and tracing different organelles.It is precisely because metal complexes have more advantages than organic compounds that the probe can be more targeted by adjusting the chemical structure.Compared with the traditional single-photon excitation emission material, the adopted two-photon excitation emission material has the advantages of strong depth resolution, small optical damage and the like,Metal complexes with two-photon absorption have great potential and broad application prospects in molecular probes and organelle imaging.With the multi-step development of many disciplines, metal complexes with two-photon absorption will be more and more widely used in chemistry, biology, medicine and other disciplines.
To sum up, many aspects should be considered when metal complexes become excellent two-photon fluorescence probes, including water solubility, cell permeability, cytotoxicity, organelle specificity, chemical and photostability, two-photon absorption cross section and so on. However, the application of two-photon technique inevitably has some limitations, such as: (1) biological samples may be (thermally) damaged due to the use of high-energy infrared/near-infrared two-photon sources; (2) Due to the high price of lasers and the inconvenience of carrying, the application cost of two-photon fluorescence probes is relatively high, and it is difficult to popularize in various research institutions and clinics. This will put forward new challenges and requirements for two-photon technology.

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Funding

the National Natural Science Foundation of China(21701113)

the Science and Technology Foundation of Shenzhen(JCYJ20190808153209537)

the Peacock Talent Fund(827-000389)

the Natural Science Foundation of SZU(2018036)

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