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Nanoscale ATP-responsive Zeolitic Imidazole Framework-90 as a General Platform for Cytosolic Protein Delivery and Genome Editing Xiaoti Yang, Qiao Tang, Ying Jiang, Meining Zhang, Ming Wang, and Lanqun Mao J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.8b11996 • Publication Date (Web): 06 Feb 2019 Downloaded from http://pubs.acs.org on February 6, 2019

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Journal of the American Chemical Society

Nanoscale ATP-responsive Zeolitic Imidazole Framework-90 as a General Platform for Cytosolic Protein Delivery and Genome Editing Xiaoti Yang,†,‡ Qiao Tang,†, Ying Jiang, † Meining Zhang, Ming Wang,†,‡* Lanqun Mao†,‡ * † Beijing

National Laboratory for Molecular Science, CAS Research/Education Center for Excellence in Molecule Science, Key Laboratory of Analytical Chemistry for Living Biosystems, Institute of Chemistry, the Chinese Academy of Sciences (CAS), Beijing 100190, China ‡ University

of Chinese Academy of Sciences, Beijing 100049, China

Department

of Chemistry, Renmin University of China, Beijing 100872, China Email: [email protected]; [email protected]. Supporting Information Placeholder ABSTRACT: Metal-organic frameworks (MOFs) are an emerging class of nanocarriers for drug delivery, owing to their tunable chemical functionality. Here we report ATP-responsive zeolitic imidazole framework-90 (ZIF-90) as a general platform for cytosolic protein delivery and CRISPR/Cas9 genome editing. The self-assembly of imidazole-2-carboxaldehyde and Zn2+ with protein forms ZIF-90/protein nanoparticles and efficiently encapsulates protein. It was found that, in the presence of ATP, the ZIF-90/protein nanoparticles are degraded to release protein due to the competitive coordination between ATP and the Zn2+ of ZIF-90. Intracellular delivery studies showed that the ZIF90/protein nanoparticle can deliver a large variety of proteins into cytosol, regardless of protein size and molecular weight. The delivery of cytotoxic RNase A efficiently prohibits tumor cell growth while the effective delivery of genome-editing protein Cas9 knocks out the green fluorescent protein (GFP) expression of HeLa cells with efficiency up to 35%. Given the fact that ATP is upregulated in disease cells, it is envisaged that the ATPresponsive protein delivery will open up new opportunities for an advanced protein delivery and CRISPR/Cas9 genome editing for targeted disease treatment.

Metal-organic frameworks (MOFs) are a class of crystalline porous materials self-assembled from metal ions and organic linkers. The “building block” approach to synthesize MOFs has enabled the precise control of chemical functionality of MOFs,1-4 which has further facilitated the biomedical application of MOFs.5-7 For instance, the tunable pore size and rigid molecular structure of MOFs allow the encapsulation of nucleic acids8-9 and proteins10-12 into MOFs, enhancing the biomacromolecule stability under harsh conditions.13-14 Moreover, nanoscale MOFs can be efficiently internalized by cells for intracellular drug delivery.15-16 Nevertheless, an efficient drug delivery using MOFs requires not only the encapsulation of therapeutics, but also the ability to release cargo into cytosol in a controlled manner.6 In this regard, controlling the self-assembly of MOFs, particularly in

response to the cellular microenvironment to promote

Figure 1. Schematic illustration of the self-assembly of ZIF-90/ protein nanoparticle, and ATP-triggered protein release from ZIF90 nanoparticle inside cells.

cargo release inside cells is highly desired for advancing MOFs-based drug delivery.8 Protein plays a critical role in regulating cell signal transduction and controlling cell fate, replacing a dysfunctional protein in disease cells has a great potential for developing precise medicine.17 Recently, the discovery of Cas9 nuclease to edit the genome of mammalian cells, denoted as CRISPR/Cas9 genome editing, has enabled the manipulation of genetic information for gene therapy.18-19 The biomedical potential of proteins, however, is largely limited by the low cell permeability of protein. Therefore, delivering protein in its active form into cells is required to fully accomplish the therapeutic potential of protein.20-22 Although MOFs have been proved to be effective carriers for protein delivery, transporting protein into cytosol, especially in response to the intracellular environment, still remains a challenge.10, 23 Herein, we report that the selfassembly of imidazole-2-carboxaldehyde (2-ICA) and Zn2+ with protein forms ZIF-90/protein nanoparticles and encapsulates protein with efficiency above 90% (Figure 1). Moreover, it was noticed that the ZIF-90/protein nanoparticles disintegrate in the presence of ATP to release protein, as a result of the competitive coordination between Zn2+ and ATP (Figure 1). ATP is present in low

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concentrations (< 0.4 mM) in the extracellular environment, but concentrated in cytosol (1 - 10 mM).24 Therefore, ZIF-

Figure 2. (a) SEM images of ZIF-90/GFP nanoparticles without (left) and with 2 mM ATP (middle) or 5 mM ATP (right) treatment. Scale bar: 100 nm; b) Normalized fluorescence of free GFP and GFP encapsulated in ZIF-90/GFP (33 μg/mL of GFP). c) Comparison of the enzyme activity of free SOD (20 U/mL of protein) and ZIF-90/SOD nanoparticles.

90 nanoparticles could be disintegrated by ATP while releasing the protein inside cells. The intracellular delivery studies indicated that the ZIF-90/protein nanoparticles can efficiently escape from endosome for cytosolic delivery of cytotoxic RNase A and genome-editing Cas9 nuclease. The ZIF-90/protein nanocomplex was prepared by directly mixing 2-ICA and Zn2+ in the presence of protein. We found that the self-assembly of ZIF-90/protein is strongly controlled by the ratio between 2-ICA and Zn2+, a high 2-ICA to Zn2+ ratio can reduce the size of ZIF-90.25 When to an aqueous solution containing 2-ICA and GFP (1 mg/mL) was added increased concentration of Zn2+, the size of resulted ZIF-90/GFP complex was decreased accordingly(Table S1). To confirm that GFP is encapsulated into the cavity of ZIF-90 nanoparticles (Figure 2a for the SEM image), the ZIF-90/GFP nanoparticles were washed with a sodium dodecylsulfate (SDS) solution, which can remove absorbed protein on ZIFs surface, followed by Fourier transform infrared spectroscopy (FTIR) characterization (Figure S1). The peaks that ascribed to GFP in the range from ~1510 to 1560 cm-1 and ~1630 to 1660 cm-1 were observed in the ZIF-90/GFP nanoparticles, but not in a simple mixture of ZIF-90 nanoparticles and GFP. A further nitrogen absorption (NAA) and thermal gravity analysis (TGA) study clearly suggested the encapsulation of GFP into ZIF-90 (Figure S2). The protein encapsulation efficiency of ZIF-90/GFP nanoparticle is higher than 90%, as determined by measuring the GFP remained in the mixture. Also, powder X-ray diffraction (PXRD) data confirmed that ZIF-90/GFP nanoparticles retained the same crystalline forms as ZIF-90 alone (Figure S3). Moreover, the direct synthesis of ZIF-90/protein nanoparticle could be generalized to encapsulate protein with different molecular weight, including bovine serum albumin (BSA) and superoxide dismutase (SOD) into ZIF90 nanoparticles (Table S2). Further characterization of these ZIF-90/protein nanoparticles was performed using FT-IR (Figure S1), PXRD (Figure S2) and dynamic light

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scattering (DLS) (Table S3). Importantly, the encapsulation of protein into ZIF-90 had a minimal effect on protein function, as evidenced by the minimal change of the

Figure 3. ATP-triggered release of GFP from ZIF-90/GFP nanoparticles. a) ZIF-90/GFP nanoparticles were treated with 1 mM and 2 mM ATP for protein release kinetics study; b) Selectivity of ATP-triggered protein release from ZIF-90/GFP nanoparticles.

dichroism spectra of GFP (Figure S4) before and after ZIF90 encapsulation. In addition, an enzyme activity assay of free SOD and ZIF-90/SOD nanoparticles shown comparable catalytic efficiency (Figure 2c), and Km and Vmax using the Michaelis–Menten kinetic model (Figure S5). We have previously found that ZIF-90 can release preloaded fluorophore in the presence of ATP, due to the competitive coordination between Zn2+ and ATP that deassembles ZIF-90.25 It was assumed that in the presence of ATP, a similar behavior could be manifested by ZIF90/protein nanoparticles. To verify this, ZIF-90/GFP nanoparticles were incubated with ATP, followed by morphology and GFP release monitoring. As shown in Figure 2a, the addition of 2 mM ATP to the suspension of ZIF-90/GFP resulted in partial disintegration of ZIF90/GFP in a short time (< 2 min.), whereas 5 mM ATP treatment caused the complete disintegration of ZIF90/GFP nanoparticles, which is also indicated by DLS measurement (Table S3). GFP release kinetics study indicated that ZIF-90/GFP nanoparticles release minimal GFP with 1 mM ATP treatment, while 2 mM ATP treatment shown 75% GFP release in 2 h (Figure 3a). More than 90% GFP was released when the ZIF-90/GFP nanoparticles was treated with 10 mM ATP (Figure 3b). Interestingly, we found a slower GFP release when the ZIF-90/GFP nanoparticle was treated with 10 mM phosphate buffered saline or under an acidic environment (Figure 3b), differentiating it from pH-responsive ZIF-8based protein delivery.10 The slower protein release from ZIF-90/GFP under acidic environment could be ascribed to the minimal ZIF-90 nanoparticle degradation, as evidenced by SEM imaging (Figure S6), which is mostly due to the interaction and encapsulation of protein into ZIF-90 changed the pH responsive property of the 2-ICA ligand of ZIF-90. Altogether, the specific ATP-dependent protein release from ZIF-90/GFP nanoparticles enables an efficient cytosolic protein delivery by making use of intracellular ATP, though the acidic subcellular compartment may also partly facilitate protein release inside cells.10 Both ZIF-90 and ZIF-90/GFP nanoparticles showed high biocompatibility for protein delivery, as revealed by


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Journal of the American Chemical Society their low cytotoxicity (Figure S7). The cellular uptake of ZIF-90/GFP nanoparticles were investigated by treating HeLa cells with the nanoparticles, followed by flow

Figure 4. Intracellular delivery of ZIF-90/GFP nanoparticles. a) cellular uptake efficiency of ZIF-90/GFP nanoparticles by HeLa cells; b) cellular uptake efficiency of ZIF-90/GFP nanoparticles in the presence of different endocytosis inhibitors; c) CLSM images of HeLa cells treated with ZIF-90/GFP nanoparticle, the endosome/lysosome was stained using LysoTracker@Red. Scale bar: 10 μm.

cytometry analysis to quantify GFP-positive cells. With the concentration of GFP increased from 40 to 100 μg/mL, the cellular uptake of ZIF-90/GFP increased proportionally (Figure 4a). More than 90% of HeLa cells were GFPpositive when they were treated with 100 μg/mL GFP, whereas free GFP treatment did not show a noticeable cellular uptake of protein. The pathway by which the ZIF90/GFP nanoparticles were internalized were subsequently studied. To this end, HeLa cells were pre-treated with four different endocytosis inhibitors, including sucrose and chlorpromazine that inhibits clathrin-mediated endocytosis, nystatin that inhibits the caveolae-mediated endocytosis, and rottlerin that inhibits the macropinocytosis, before ZIF90/GFP delivery. The cellular uptake efficiency of ZIF90/GFP by the pre-treated cells was compared to those untreated with endocytosis inhibitors.26 With the pretreatment of endocytosis inhibitors, only sucrose significantly reduced the cellular uptake efficiency down to 17% of that without any pre-treatment (Figure 4b), indicating that the ZIF-90/GFP nanoparticles are mainly internalized by cells via clathrin-mediated endocytosis. The intracellular localization of ZIF-90/GFP was further studied by confocal laser scanning microscopy (CLSM) imaging. After the treatment of HeLa cells with 50 μg/mL ZIF90/GFP nanoparticles, a significant accumulation of GFP in the cytosol was noticed (Figure 4c). In addition, the costaining of endosome/lysosome indicated that most of ZIF90/GFP nanoparticles were escaped from endosome, and released GFP into cytosol. We hypothesized that the efficient endosome escape of ZIF-90/GFP could be ascribed to the protonation of the 2-ICA of ZIF-90 within the acidic endosome that drives a “proton sponge” effect,27

a well-known pathway for the endosome escape of nanoparticles. We next studied the use of ZIF-90 nanoparticle for cytosolic delivery of functional protein, and its potential for developing new protein therapy. We first investigated the delivery of a chemically-modified protein, RNase A-NBC, that shows selective cytotoxicity against cancer cells.28-29 To address this challenge, RNase A-NBC was encapsulated in ZIF-90 nanoparticles in a similar manner by which GFP protein was loaded in this MOFs(Table S2). Afterwards, HeLa cells were treated with the ZIF-90/RNase A-NBC nanoparticles, and compared to cell with free RNase ANBC treatment. Free RNase A-NBC manifested very weak cytotoxicity at all protein concentrations we studied (Figure 5a), on the contrary, ZIF-90/RNase A-NBC nanoparticles showed an enhanced cytotoxicity against HeLa cells. For instance, the treatment of HeLa cells with ZIF-90/RNase A-NBC, which corresponds to 135 μg/mL RNase A-NBC, reduced cell viability to 15%, emphasizing the high efficiency of ZIF-90 nanoparticle to deliver cytotoxic proteins for cancer therapy. To confirm the essential role of ATP on promoting cytosolic RNase A-NBC delivery, we pre-treated HeLa cells with 2- deoxy-glucose (2-DOG), which can reduce intracellular ATP before ZIF-90/RNase A-NBC delivery. The pre-treatment of 10 mM 2-DOG reduced intracellular ATP concentration down to 50% of that without 2-DOG pretreatment (Figure S8). Cytotoxicity assay indicated that 2-DOG and ZIF-90/RNase A-NBC cotreated cells shown less cell growth inhibition than that only treated with ZIF-90/RNase A-NBC, suggesting that ATP can promote protein release from ZIF-90/RNase ANBC and to enhance cytotoxicity of RNase A-NBC.

Figure 5. Cytosolic delivery of functional proteins using ZIF-90 nanoparticles. a) RNase A-NBC delivery efficiently prohibited tumor cell growth; b) the delivery of ZIF-90/Cas9 nanoparticle efficiently knocked out GFP expression of HeLa-GFP cells . HeLa-GFP cells were treated ZIF-90/Cas9 nanoparticles (120 nM Cas9) alone with 60 nM sgRNA.

Lastly, investigating the potential of ZIF-90 as effective protein carriers was extended to Cas9 nuclease delivery for genome editing. The biomedical potential of CRISPR/Cas9 genome editing depends on the delivery of Cas9 protein and single-guide RNA for subsequent genetic information manipulation.19,30-32 To demonstrate the potential of ZIF-90 for genome-editing protein delivery, a genetically fused Cas9 and GFP protein, Cas9-EGFP was self-assembled into ZIF-90 and added to HeLa cells. The delivery of 45 nM Cas9-EGFP resulted in 60% GFP-positive cells (Figure S9), while Cas9-EGFP alone shown very weak cellular uptake efficiency. To further study the potential of ZIF-



90/Cas9 nanoparticle delivery for genome editing, HeLa cells stably-expressing GFP were transfected with ZIF90/Cas9 nanoparticles, followed by the delivery of sgRNA targeting GFP using commercial Lipofectamine 2000. An efficient delivery of Cas9/sgRNA and an on-target cleavage of GFP gene could result in the loss of cell fluorescence. As shown in Figure 5b, ZIF-90/Cas9 nanoparticle treatment efficiently knocked out the GFP expression of HeLa-GFP cells up to 40% compared to non-treated HeLa cells, indicating an effective CRISPR/Cas9 genome editing upon ZIF-90/Cas9 nanoparticles delivery. In summary, we report herein the self-assembly of ZIF90/protein nanoparticles as a general platform for cytosolic delivery of native and functional protein. The encapsulation of protein into ZIF-90 nanoparticle is not dependent on protein size and molecular weight, and pre-loaded protein is efficiently released in the presence of physiological concentration of ATP. Due to the abnormal ATP level in disease cells, we believe that the ATP-responsive protein delivery described herein not only expands the chemistry of MOFs for advanced biomedical applications, but also opens up new opportunities for an advanced protein delivery, and an advanced CRISPR/Cas9 genome editing technique for targeted disease treatment.

ASSOCIATED CONTENT Supporting Information Experimental details, characterization and intracellular delivery study of ZIF-90/protein nanoparticles. The Supporting Information is available free of charge on the ACS Publications website at xxx.

AUTHOR INFORMATION Corresponding Author *[email protected]; *[email protected].

Notes The authors declare no competing financial interest.

ACKNOWLEDGMENT We acknowledge generous financial support from the National Key Research and Development Program of China (2017YFA0208100 to MW, 2016YFA0200104 to LM), the National Science Foundation of China (21778056 to MW; 21790390, 21790391, 21621062 and 21435007 to LM).

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