Supplementary Information (SI)
Scheme S1: Folic Acid conjugation with bovine serum
Scheme S2: Folic Acid-BSA conjugated with PEG forming HPNP-FA carriers
Table S3: Fluorescent markers of nucleotides, polypeptide and capsules
Zeta potential measurements
The zeta potential surface of HPPNC and HPPNC- FA was measured by using a Malvern Nano ZS90 (Malvern Instruments, UK). The mean of five successful runs were considered for analysis.
Table S4: Properties of HPNP-FA compared to HPNP.
Activation of carboxylic group of folic acid
As already reported in literature, FA has good solubility in DMSO (Laing et al., 2011) and limited solubility in distilled water (e.g. see Fig. S5A). The maximum absorption peaks of folic acid at 280 and 360 nm can be used to confirm the covalent attachment of the folate with nanoparticles (Pan et al., 2003).The UV visible absorption results reveals a weak peak at 280 nm for FA mixed with D.W. On the contrary, FA dissolved in DMSO shows good absorption peaks at 280nm and 360 nm (Liu et al., 2010) (e.g. see Fig. S5B). DMSO is able to dissolve hydrophilic and hydrophobic solutes (Clark et al., 2008) and it can participate in the reaction (Diao et al., 2012). This justifies the employment of DMSO in our studies as a good solvent for reaction involving FA (Laing et al., 2011).In Fig. S5C FTIR spectra of FA dissolved in D.W. show that bands at 3553 and 3412cm−1 are due to the hydroxyl (OH) stretching bands of glutamic acid moiety and NH group of pterin ring. The stretching vibration peak of C=O appears at 1707 cm−1, while the band at 1602cm−1 is assigned to the bending mode of NH vibration. The band 1496 cm−1 is attributed to characteristic absorption band of the phenyl and pterin ring (Zhang et al., 2008). There is no absorption locates at range from 2600 to 2000 cm-1 (He et al., 2009). FTIR spectra of FA dissolved in DMSO shows that 3271 cm-1 and 3141 cm -1 bands are assigned to shifting of hydroxyl group band due to the proton transformation. More importantly, a new mid-strong absorption band appears at 2354cm−1, and it is ascribed to N+–H stretching vibration band of C =N+H– on pterin ring. This might be due to protonate N atom of pterin ring (He et al.,2009). This may explain the importance of DMSO in reaction involved FA whereas it probably facilitates transfer proton from carboxyl at glutamic acid moiety to N atoms at pterin ring. Hence, it is well known that the lone-pair electrons on N atoms at pterin ring are not conjugated with ring π system, so they are capable to combine with proton to produce positive salt (Hammud et al., 2010). Band of C=O might be shifted to 1731 cm−1. The characteristic bands of the phenyl and pterin ring are assigned to 1531 and 1519 cm-1 wavelengths, respectively. In the presence of EDC, FA–COOH was cleaved and its carboxylic group joined to oxygen of N-hydroxy succinimide by single bond forming N-hydroxy succinimide ester of folic acid (e.g. see Scheme S1). The successful folic acid esterification was detected by two main characteristic bands 1731 and 1660 cm-1 (see Fig.S5Cactivated FA). They are assigned to C=O and C=C stretching vibration.In Fig. S5D respect to no fluorescence intensity coming out from folic acid mixed with distilled water, FA dissolved by DMSO shows good fluorescence intensity emission at 450 nm (Uyeda and Rabinowitz, 1963). Also activated FA gives similar fluorescence emission intensity compared to FA. Absorbance and fluorescence peaks that may characterize folic acid spectrum are due to the aromatic ring of its chemical structure (Wilson and Jacobson, 1977).
Figure S5: Spectroscopic behaviour of Activated folic acid A) Photograph of folic acid dissolution process; B) Folic Acid absorbance; C) FTIR spectra of Folic Acid; D) Fluorescence intensity of Folic Acid.
References
1. B.M. Laing, P. Guo and D.E. Bergstrom Methods 2011, 54, 260.
2. D. Pan, J. L. Turner, K. L. Wooley Chem. Commun. 2003, 19, 2400.
3. F. Liu, D. Deng, X. Chen, Z. Qian, S. Achilefu and Y. Gu.Mol Imaging Biol 2010, 12, 595.
4. T. Clark, J.S. Murray, P. Lane and P. Politzer, J. Mol. Model. 2008,14,689.
5. T. Diao, P. White, I. Guzei and S.S.Stahl Inorg.Chem. 2012, 51, 11898.
6. J. Zhang, S. Rana, R.S. Srivastava and R.D.K. Misra Acta Biomaterialia 2008, 4, 40.
7. Y.Y. He, X.C. Wang, P.K. Jin, B. Zhao and X. Fan Spectrochimica Acta Part A 2009,72, 876.
8. Kafa Kh. Hammud, Ali G. Ahmed Abdul Latif M. Raouf, Riyadh R. Neama, Muhaned Z. Abdul Rahman Diyala Journal for pure science 2010, 6, 71.
9. K. Uyeda and J.C. RabinowitzAnal. Biochem. 1963, 6,100.
10. T.G. Wilson and K. Bruce Jacobson Biochemical Genetics 1977, 15, 307.
Figure S6: Spectroscopic behaviour of fluorescent labeling and nucleotides markers. A) R6G; B) free capsule; C) encapsulated SHT- DNA; D) encapsulated siRNA; E) Encapsulated P-17; F) siRNA encapsulated without capsules labeling; G) P-17 encapsulated without capsules labeling.
Both free HPPN-FA carriers and encapsulated SHT-DNA show peak at ~550 nm (e.g. see Fig. S6(B-C)) because they are attached to R6G. Encapsulated Alexa Flour-siRNA inside FITC labeled HPPNCs carrier gives emission at ~510 nm (crf. Fig. S6D), whereas in case of absence HPPNCs-FA marker, Alexa Flour-siRNA gives a weak emission at ~570 nm (e.g. see Fig. S6F). Peptide-17 conjugated with R6G and encapsulated inside FITC labeled HPPN-FA presents two close peaks at ~510 and 550 nm (see Fig. S6E). They are related to the emissions of FITC and R6G respectively, whereas peptide-17 attached to R6G encapsulated inside HPPN-FA without labeling by FITC, gives peak at 550 nm (see Fig. S6G).
Agarose gel electrophoresis
FA-derived complexes were run on an agarose gel electrophoresis. The separation depended on their ability to move through a conductive medium in response to an applied electric field.
1.5 % agarose gel was prepared. 16µl of each sample, namely FA dissolved in ddH2O, FA dissolved in DMSO, activated FA, HPPNC and HPPNC-FA and Free capsules, SHT-DNA, siRNA and P-17- were mixed with 4 µl of a solution of Orange G dye in glycerin. The gel were run at 60 volt for 30 min. Then they were analyzed by using BioRad Gel Doc XR system by using two filters: (520±15 nm and 560±25 nm).
Figure S7: Gel electrophoresis characterization of HPNP moieties (A-C) and encapsulated nucleotides and polypeptide (D-E).
Panels D-E of Fig. S7 show gel electrophoresis characterization of biomolecules (short DNA, siRNA) and peptide-17) prior and after encapsulation into the carrier. Free P-17, as expected, does not show any fluorescence band under 515 and 560 nm filters. Free SHT-DNA conjugated with GFP gives fluorescent band under both filters (e.g. line 2). Free siRNA conjugated with Oligo Alexa Flour shows fluorescence band in both filters (see line 3). Capsules labeled by R6G exhibits fluorescent band at 560 nm filter (line 4). Encapsulated SHT-DNA exhibits fluorescence band under 560 nm filter (see line 5) and is related to emission of R6G (at 550 nm). Even encapsulated P-17 attached to R6G shows fluorescence band using 560 nm filter (e.g. line 6), whereas the carrier labeled by FITC exhibits fluorescence band at 520 nm filter (e.g. line 6). Encapsulated siRNA conjugated with Alexa Fluor shows fluorescence band using 520 nm filter (see line 7). This band might be overlapped with emission of FITC labeled capsules.
siRNA attached with Alexa flour that was encapsulated at unlabeling capsules, gives fluorescence band related to Alexa flour (see Fig. S7F, line 7). This indicates that FITC and Alexa flour were running in the same direction.
X-ray diffraction analysis
10 µl of BSA, BSA-FA, FA dissolved in ddH2O and HPPNC-FA were dropped separately into clean silicon wafer substrate and allowed drying overnight. The measurements were performed by Cu Ka (λ = 1.5405 Å) X-ray diffraction scans were taken in the large angle (10° to 50°) θ/2θ mode by using a PANalytical X’Pert-PRO Materials Research Diffractometer.
Figure S8: X-ray diffraction (A) and ELISA fluorescence spectrum (B) (folic acid crystallography and fluorescence emission).
Diffraction study showed two peak locates at ~ 16° and ~ 22° (e.g. see Fig. S8A, free FA spectrum). They are correlated to diffraction of FA crystals [Florea et al. 2012], whereas there is no peak emerging from BSA sample alone[Irene Russo Krauss et al. 2012]. This is due to the low diffraction power of its crystals[Irene Russo Krauss et al. 2012]. However, diffraction of folic acid conjugated with BSA exhibits several peaks between 12° and 30°. One of them shows entrapped spectrum of folic acid at ~ 21,6° (see Fig. S8A, FA+BSA). The successful integration of folic acid among BSA structure allows for designing protein-ligand interaction at a structural level and providing possibility to functionalize protein structure. Similarly, the diffraction peak of HPPNCs-FA emerges at ~ 21,6° (e.g. see Fig. S8A, HPPNCs-FA). This indicates that FA crystallography might not be changed after mixing with PEG, since carboxylic groups of folic acid were occupied by its reaction with BSA.
References
1. M.G. Florea, A. Ficai, O. Oprea, C. Guran, D. Ficai, L. Pall, and E. Andronescu, REV ROM MATER, 42 (2012) 313-316.
2. Irene Russo Krauss , Filomena Sica Carlo Andrea Mattia and Antonello Merlino Int. J. Mol. Sci. 13, (2012),3782-3800.
Cellular uptake
HLF Cell lines were seeded on sterilized glass coverslips into 4 glass-bottomed petri dishes, with density of 2000 cells for each one. They were grown in DMEM High Glucose (4,5 g/l) supplemented with 5% L-Glutamine, 10% fetal bovine serum, 5% penicillin-streptomycin and 5% sodium pyruvate in a humidified atmosphere of 37°C, 5% CO2. After 24 h, 200 µl of each encapsulated samples (Free capsules, SHT-DNA, siRNA and P-17) were added. Cellular uptake was measured by confocal microscope after 72 h incubation.
Figure S9: Confocal Microscopy photomicrographs of nano-carriers cellular uptake and nucleotides transcription (scale bar 20µm).
In Fig. S9 the cellular internalization of carriers encapsulating SHT-DNA, siRNA and P-17 was determined by confocal microscopy. GFP-code sequence of SHT DNA revealed green fluorescence intensity after internalization. This finding may explain why this intensity is not being detected after their encapsulation by fluorescence spectrophotometer or agarose bio analyzer. Additionally, The expression of GFP indicates that SHT DNA was successfully encapsulated and localised in the cytoplasm. siRNA conjugated with Alex Fluor is located at cytoplasm and nucleus. Alex Fluor-siRNA indicated good appearance by exhibiting its emission intensity at 546nm wavelength. Their emission gives rise to red color in TRITC channel. Furthermore, encapsulated P-17 exhibits red color in TRITC channel because it is labeled by R6G.
Western Blot Analysis
Total protein extracts were obtained as described previously [23], separated by SDS/PAGE (12% polyacrylamide gels) and transferred on to PVDF membranes. After blocking with 5% (w/v) non-fat milk TBST [Tris-buffered saline solution containing 0.05% (v/v) Tween 20] the membranes were incubated overnight with the corresponding antibody in a 0.5% non-fat milk TBST (diluted 1:5000 for β-actin and 1:1000 for all others). After washing and incubating the membrane with an appropriate peroxidase-conjugated antibody (diluted 1:5000) for 1 h at 21°C, antibody binding was revealed using ECL® (GE-Healthcare). β-actin was used as a loading control.
Figure S10: Western Blot Analysis.Effect of encapsulated P-17 on phosphorylation of SMAD2 with exogenous TGF and without TGF into HEP3B and SNU449 cell lines.
Uptake of Hybrid polymeric protein nanocarrieres (HPPNCs) by Breast and Ovarian Cancer cells investigated by Confocal Laser Scanning Microscopy (CLSM).
MCF-7 (breast cancer) and OVCAR-3 (ovarian cancer) cell lines were purchased by ATCC and cultured as described in materials and methods § 3.1.
Figure S11: CLSM images of HPPNCs-FA internalised A) in MCF-7 cell line ; B) in OVCAR-3 cell line; C) high magnification of A); D) high magnification of B).
HPPNCs-FA were synthetised as reported in § 2.1 and stained by FITC (green color) while for nuclear staining, fixed cells were mounted with DAPI-conjugated medium.
Internalization of HPPNCs-FAin MCF-7 (breast cancer) (see Figure S11A-C) and OVCAR-3 (ovarian cancer) cell line (see Figure S11B-D) after their incubation for 24h was investigated by means of Confocal Laser Scanning Microscopy. The images of fluorescently labeled proteins were acquired by using a confocal laser-scanning microscope (CLSM) (TCS-SP5, Leica, Germany). Confocal images shows successful uptake of HPPNCs-FA by both cancer cell lines (see Figure S11C, high magnification and Figure S11D, high magnification).
These CLSM images demonstrate clearly that FA integrated nano-carriers can be targeted toany type of cancer cells having expression to folate receptors, not only HCC cells. However, internalization capacity of FA-nanosystem depends on high overexpression of folate on cancer cell surface.