Next Article in Journal
In Situ “Humanization” of Porcine Bioprostheses: Demonstration of Tendon Bioprostheses Conversion into Human ACL and Possible Implications for Heart Valve Bioprostheses
Next Article in Special Issue
In Situ Quantification of Polyhydroxybutyrate in Photobioreactor Cultivations of Synechocystis sp. Using an Ultrasound-Enhanced ATR-FTIR Spectroscopy Probe
Previous Article in Journal
The Role of Collagen-Based Biomaterials in Chronic Wound Healing and Sports Medicine Applications
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Bioengineering
Volume 8
Issue 1
10.3390/bioengineering8010009
bioengineering-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Antioxidant Network Based on Sulfonated Polyhydroxyalkanoate and Tannic Acid Derivative

by
Laura Brelle
,
Estelle Renard
and
Valerie Langlois
*
Univ Paris Est Creteil, CNRS, ICMPE, UMR 7182, 2 rue Henri Dunant, 94320 Thiais, France
*
Author to whom correspondence should be addressed.
Bioengineering 2021, 8(1), 9; https://doi.org/10.3390/bioengineering8010009
Submission received: 10 November 2020 / Revised: 22 December 2020 / Accepted: 23 December 2020 / Published: 8 January 2021
(This article belongs to the Special Issue Advances in Polyhydroxyalkanoate (PHA) Production, Volume 3)
Browse Figures
Review Reports Versions Notes

Abstract

:
A novel generation of gels based on medium chain length poly(3-hydroxyalkanoate)s, mcl-PHAs, were developed by using ionic interactions. First, water soluble mcl-PHAs containing sulfonate groups were obtained by thiol-ene reaction in the presence of sodium-3-mercapto-1-ethanesulfonate. Anionic PHAs were physically crosslinked by divalent inorganic cations Ca2+, Ba2+, Mg2+ or by ammonium derivatives of gallic acid GA-N(CH3)3+ or tannic acid TA-N(CH3)3+. The ammonium derivatives were designed through the chemical modification of gallic acid GA or tannic acid TA with glycidyl trimethyl ammonium chloride (GTMA). The results clearly demonstrated that the formation of the networks depends on the nature of the cations. A low viscoelastic network having an elastic around 40 Pa is formed in the presence of Ca2+. Although the gel formation is not possible in the presence of GA-N(CH3)3+, the mechanical properties increased in the presence of TA-N(CH3)3+ with an elastic modulus G’ around 4200 Pa. The PHOSO3−/TA-N(CH3)3+ gels having antioxidant activity, due to the presence of tannic acid, remained stable for at least 5 months. Thus, the stability of these novel networks based on PHA encourage their use in the development of active biomaterials.

1. Introduction

Poly(3-hydroxyalkanoate)s (PHAs) are natural polymers produced by microorganisms as carbon and energy storage compounds when they are placed under special growth conditions. PHAs are naturally occurring aliphatic polyesters that have a high structural diversity related to the alkyl pendant group [1,2,3]. The length of this side chain group is decisive for their final thermal and mechanical properties. PHAs can be divided into three main types depending on the number of carbon atoms in the monomer unit: short-chain-length PHAs (scl-PHA), with monomers consisting of 3–5 carbon atoms, medium-chain-length PHAs (mcl-PHA), with monomers consisting of 6–14 carbon atoms, and long chain length PHAs (lcl-PHA), which are obtained from long chain fatty acids with more than 14 carbon atoms. The former display physical properties associated with highly crystalline thermoplastics while the latter generally possess low crystallinity and elastomeric character. Due to their biodegradability [4,5] and biocompatibility, they constitute a very promising group of natural biomaterials for various biomedical applications including drug delivery and tissue engineering [6,7,8,9].
In order to enlarge the potential in biomedical applications, chemical modifications of mcl-PHAs have been performed. One of the first studies concerning the chemical modification of PHAs started with the production of poly(3-hydroxyoctanoate-co-3-hydroxyundecenoate) (PHOU) that contained unsaturated groups in the side chains [10,11]. The chemical modifications of the unsaturated groups of PHOU have already been reported [12,13,14,15,16,17]. The introduction of polar groups, such as hydroxyl, carboxylic and ammonium groups, makes it possible to modify the hydrophilic/hydrophobic balance of the polymer. Amphiphilic PHAs-PEG copolymers that were synthesized by esterification [18,19,20] and by click chemistry [21,22,23,24] have shown the ability to self-associate in aqueous medium to form micelles, vesicular structures or polymersomes. Water soluble PHAs obtained by introducing PEG [18], ammonium groups [25], or sulfonate functions [26,27] retained their biocompatible and non-cytotoxic character and the presence of PEG and propyleneglycol (PPG) segments provided hydrophilicity, blood compatibility [28], and thermo-sensitivity respectively [29,30].
Networks based on PHAs were prepared by photoactivated reaction in the presence of PEG-monoacrylate [28] or PEG-diacryloyl [31]. Chen et al. [32] recently reported PHA gel via photo-crosslinking based on a thiol-ene reaction with PEG-dithiol as a photo-cross-linker. Although some structures from chemically cross-linked PHAs have already been described in the literature, there is to our knowledge no study on the gels with PHAs bearing sulfonate groups. These novel materials should constitute an interesting support in the biomedical field because of the biological interactions of the sulfonate groups due to their anticoagulant, antiangiogenic, and antimitogenic properties. These active anionic sites are known to interact with proteins, such as fibronectin [33,34,35,36].
In our paper, we describe the synthesis of PHA sulfonate, PHOSO3−, by a photoactivated thiol-ene process in the presence of sodium-2-mercapto-1-ethanesulfonate and the elaboration of crosslinked structures by combination with bivalent cations or organic polycationic molecules (Figure 1).
Among the bivalent cations that have the capability of forming a gel by ionic interactions with anionic polymers, Ca2+, Ba2+, and Mg2+ present interesting properties in biomedical applications [37,38,39]. In particular, the gelation of an alginate solution with a multivalent ion of opposite charge such as Ca2+ allows to obtain a resistant and biocompatible hydrogel.
To increase the numbers of ionic interactions, we report here the synthesis of ammonium derivatives of gallic acid and tannic acid. Gallic acid (GA) is a natural tri-hydroxybenzoic acid extracted from plants and evaluated as an antioxidant, antibacterial, and antiviral compound [40,41]. Tannic acid (TA) is a kind of natural polyphenol that is commonly found in high herbaceous and woody plants that is a well-known bio-based molecule for its antioxidant and antibacterial activity [42,43,44]. Moreover, polyphenols due to their cyclic structure and the presence of a large content of hydroxyl groups are good candidates for the development of stable physical gels and offer the possibility to be easily modifiable through these accessible functions. Tannic acid has already shown the ability to make gels or hydrogels with good mechanical structures by different interactions such as supramolecular interactions by hydrogen bonds [45], coordination with transition metals [46,47], and a self-assembly method by redox reaction [48,49]. A series of biobased UV-curable antibacterial resins were synthesized through modifying tannic acid with glycidyl methacrylate (GMA) [50]. In this study, ammonium groups were introduced on GA and TA through reaction with glycidyl trimethyl ammonium chloride (GTMA). The presence of ammonium groups on GA and TA increases both the number of cationic charges compared to divalent cations and the rigidity by the presence of the aromatic rings. Gels were formed by ionic interactions of the oppositely charged polyelectrolytes PHOSO3− and Ca2+, Ba2+ and Mg2+, and GA-N(CH3)3+ and TA-N(CH3)3+. The viscoelastic properties of the gels and their antioxidant activity were studied.

2. Materials and Methods

2.1. Materials

Poly(3-hydroxyoctanoate-co-3-hydroxyundecenoate) with 33% double bonds PHOU was provided from the Swiss Federal Laboratory for Materials Testing and Research (EMPA, Switzerland, Mn = 40,000 g/mol, Polydispersity index 1.7). The different comonomers are randomly distributed. CaCl2, BaCl2, MgCl2, and Sodium 2-mercapto-1-ethanesulfonate (98%) were purchased from Aldrich. Tannic acid was purchased from Alfa Aesar. Tetrahydrofuran (THF), dimethylsulfoxide (DMSO), methanol, and ethanol absolute anhydrous were purchased from Carlo Erba. Gallic acid, 2,2-dimethoxy-2-phenylacetophenone (DMPA, Irgacure 651), glycidyltrimethyl ammonium (GTMA), triphenylphosphine (TPP), and methyl hydroxyquinone (MEHQ), were supplied from Sigma-Aldrich and were used without prior purification. Butylacetate was supplied from Merck. Tannic acid was purchased from Alfa Aesar.

2.2. Synthesis of PHO Sulfonate, PHOSO3−

A total of 0.2 g PHOU was solubilized in 12 mL THF under agitation at room temperature. Five molar equivalents (relative to the double bonds of PHOU) of sodium 2-mercapto-1-ethanesulfonate (98%) and 0.5 eq. molar DMPA were solubilized in 18 mL of a MeOH/THF (2/1 v/v) mixture. The mixture placed at 11 cm was irradiated for 300 s at room temperature with a mercury xenon (180 Mw·cm−2) Lightning cure LC8 (L8251) lamp from Hamamatsu coupled with a flexible light guide. During the entire irradiation process the mixture was kept under stirring. After irradiation, 25 mL DMSO was added. The resulting product was dialyzed in a 1000 Da cut-off dialysis tube against distilled water, which was changed three times daily for 4 d.

2.3. Synthesis of Trimethyl Ammonium Gallic Acid: GA-N(CH3)3+

In a two-neck round-bottom flask, 2.125 g of gallic acid, 4.996 × 10−2 moles of GTMA, 0.1456 g of triphenylphosphine (TPP) and 0.0097 g of methyl hydroxyquinone (MEHQ) were solubilized in 5 mL of anhydrous ethanol and butyl acetate 1:2 (v:v), under an inert atmosphere. The mixture was stirred at 100 °C for 48 h. After 48 h, the mixture was precipitated in acetone to remove solvent and then purified by flash column chromatography using methanol as an eluent.

2.4. Synthesis of Trimethyl Ammonium Tannic Acid: TA-N(CH3)3+

In a flask, 4.25 g of tannic acid, 0.25 moles of GTMA, 0.09 g of triphenylphosphine (TPP) and 0.0075 g of methyl hydroxyquinone (MEHQ) were solubilized in 10 mL of an anhydrous ethanol and butyl acetate 1:2 (v:v) mixture, under an inert atmosphere. The mixture was stirred at 100 °C for 48 h. Then it was solubilized in an H2O/ethanol mixture (25:75) and centrifuged. The precipitate containing the TA-N(CH3)3+ was recovered and dried in a vacuum chamber at 40 °C for one night. The molar mass of the monomeric unit of the polymer is M0 = (0.67 × 142) + (0.33 × 323) = 201 g·mol−1.

2.5. Elaboration of Network Based on PHOSO3−

PHOSO3−/Ca2+. Networks were prepared according to the following protocol. A total of 0.05 mL of CaCl2 0.2 M was added to 0.25 mL of PHOSO3− with a concentration of 27 g·L−1. The mixture was vortexed for 30 s allowing the instantaneous formation of the network.
PHOSO3−/TA-N(CH3)3+. A total of 0.2 mL of PHOSO3− with a concentration of 96 g·L−1 and 0.01 g of TA-N(CH3)3+ were introduced into a haemolysis tube. After an agitation with a vortex, a sticky, brown gel was formed.

2.6. DPPH Test

The radical scavenging activity (RSA) of the networks was determined by using 2,2-diphenyl-1-picrylhydrazyl. A total of 37 mg of the PHOSO3−/TA-N(CH3)3+ were immersed in 3 mL of 0.1 mM of DPPH solution in methanol in the dark for 60 min at room temperature. The RSA was measured by using a Varian Cary 50 Bio UV-Visible spectrophotometer controlled by the CaryWinUV software. RSA was therefore determined by monitoring the decrease of the absorbance at 517 nm (Equation (1)):
RSA (%) = ((Aref − As)/Aref) × 100
where Aref corresponds to the absorbance of the 0.1 mM of DPPH solution without a sample and As corresponds to the absorbance of the 0.1 mM solution of DPPH with 37 mg samples of tannic derivatives.

2.7. Characterization

The molar mass of the PHO(67)U(33) was determined by Size Exclusion Chromatography in THF using a Schimadzu LC-10AD pump with two Shodex GPC K-805L columns (5 µm Mixte-C) at a concentration of 10 mg·mL−1. A Wyatt Technology Optilab Rex interferometric refractometer (Toulouse, France) was used as a detector, and low polydispersity index polystyrene standards (3 × 104–2 × 106 g/mol) were used for PHOU analysis. 1H NMR spectra (400 MHz) were performed with a Bruker AV 400M spectrometer (Wissembourg, France). In a disposable spectrophotometer cell, 10 µL of CaCl2 (0.2 M) was added to 0.250 mL of PHOSO3− at 37 g·L−1, in a constant manner. After manual stirring, the transmittance was measured at 600 nm with a UV-vis Cary50 Bio Varian UV−visible spectrometer supplied by Varian (Agilent, Les Ulys, France) recording controlled by Cary Win UV software in the range 250–800 nm. Rheological properties were determined with a hybrid rheometer (DISCOVERY HR-2) (Guyancourt, France) using a cone and plate geometry (20 mm, 1°). Rheological tests were performed at 25 °C (room temperature) and the Peltier temperature control system was used to keep the temperature constant throughout the analysis. The evaporation of the water contained in the 3D network was limited by the presence of a solvent trap. For PHOSO3−/M2+ networks, the elastic modulus (G’) and viscous modulus (G”) were plotted against frequency from 0.1 et 100 rad·s−1 for an applied strain at 20% on 0.350 mL of a 3D network. In addition, for the PHOSO3−/TA-N(CH3)3+ network frequency sweep tests were done between 0.1 and 100 Hz for an applied strain at 1%. These measurements were carried out three times to ensure the repeatability of the results and the viability of the tests.

3. Results and Discussion

3.1. Synthesis of Poly(3-Hydroxyalkanoate) Sulfonate, PHOSO3−, Ammonium Derivatives of Gallic Acid GA-N(CH3)3+ and Tannic Acid, TA-N(CH3)3+

Poly(3-hydroxyoctanoate-co-3-hydroxyundecenoate) PHOU is a hydrophobic polyester composed of long alkyl side chains and lateral unsaturated groups. Sulfonate groups were grafted to the terminal double bonds of the PHOU, to both provide an amphiphilic character to the PHA and to induce non-covalent binding of SO3− ions to cationic species to form ionic crosslinking (Figure 1).
Poly(3-hydroxyoctanoate-co-3-hydroxyundecenoate), PHOU was first characterized by 1H NMR (Figure 2) to determine the percentage of terminal unsaturation by integrating protons corresponding to the CH peak (2) at 5.1 ppm, and the signal relating to the terminal alkene group of side chain (7) at 5.7 ppm. Sodium-3-mercapto-1-ethanesulfonate was grafted under photochemical activation, using 5 molar equivalents of sulfonate groups. After purification by dialysis, the polymers were dried by freeze-drying and then analyzed by 1H NMR. The presence of the signals relating to the two CH2 methylene (c, d), which are characteristic of sulfonate groups, appeared at 2.66 ppm and the total disappearance of the peaks relating to the terminal alkene group of side chains (7) and (8) indicated the success of the formation of PHOSO3−. We previously showed that no chain scission occurred during this thiol-ene reaction and the PHOSO3− is water soluble [26,27].
Ammonium derivative of gallic acid GA-N(CH3)3+ and tannic acid TA-N(CH3)3+ were synthesized through the reaction with glycidyl trimethylammonium chloride GTMA (Figure 3). 1 H NMR spectra (Figure 4) showed that GTMA was grafted to phenol groups of the TA due to the disappearance of the peak at 3.1 ppm (a) which correspond to the epoxide groups of GTMA and the appearance of peaks at 3.5–4.6 ppm, which correspond to the -CH2-CH(OH)-CH2-N(CH3)+ units (a’, b’, c’). The number of ammonium groups N(CH3)3+ was calculated from the area ratio of the peaks at 6.7–7.5 ppm (I1,2), which corresponds to the protons on the aromatic group of tannic acid, and the peak at 3.2 ppm (Id), which are characteristic of the protons on the ammonium groups (Equation (2)). The conversion of the grafting reaction is defined by Equation (3).
N ( CH 3 ) 3 + = I 1 , 2   × 20 I d   × 9
Conversion   ( % ) = N ( CH 3 ) 3 + 25   × 100
The substitution degree of TA was calculated as around 76% (which corresponds to 19 N+ per molecule) and TA-N(CH3)3+ is totally soluble in water. The substitution reaction of GA determined by NMR is quantitative. The degree of substitution was calculated as the ratio of the integration of the peak (d) at 3.3 ppm to the number of hydrogens carried by the nitrogen atom (N+), i.e., nine. Integration of peaks b and c confirmed that there were 4 N+ per molecule. As a consequence, we can further study the influence of the numbers of ammonium groups on the gel formation.

3.2. Effects of the Nature of Cations on the Formation of Gels

Networks were spontaneously formed after a few seconds of mixing PHOSO3− and cationic species. The influence of the nature of divalent cations as Mg2+, Ba2+, and Ca2+ was first studied. In the presence of Mg2+ no gel formation was observed regardless of the concentration. Mg2+ therefore does not have sufficient interaction energy and attractive power [51]. The Ba2+ did not allow the formation of a gel and gave rise to a precipitate even at very low concentrations. This result may be due to the bigger size of the barium atom nucleus combined with an insufficient proportion of sulfonate functions [52]. PHOSO3−, which is completely soluble in water (27 g·L−1; 1.1 × 10−5 moles), instantly forms a network in the presence of a sufficient molar concentration of Ca2+. The variation of transmittance as a function of the number of moles of Ca2+ showed three well-defined zones (Figure 5). A first zone is defined between 0 to 1.5 × 10−5 moles, showing that the polymer remains in solution. Between 1.5 × 10−5 and 2.5 × 10−5 moles, the transmittance drops sharply from 98% to 20%, respectively, attesting to the gel formation. The addition of Ca2+ beyond this concentration does not modify the transmittance, which remains constant at 20%. The presence of precipitate is then observed when the moles of salt are greater than 2.6 × 10−5 moles.
The gel formation conditions were studied next in the presence of Ca2+, gallic acid and tannic acid derivatives. Under our conditions, no gel was formed in the presence of GA-N(CH3)3+ whereas gels formed very easily in the presence of TA-N(CH3)3+, which allows us to affirm that the number of positive charges is very important during gel formation. Therefore, in order to be able to compare the conditions of gel formation in the presence of Ca2+ and the TA-N(CH3)3+ derivative, Figure 6 shows the different zones observed for the gels as a function of the number of positive and negative charges. To perform this study we added increasing volumes of positive charge solution (Ca2+ or TA-N(CH3)3+) from the same initial solution. The results obtained are very different because there are three zones in the case of Ca2+ (liquid, gel and precipitate), whereas there are only two zones for TA-N(CH3)3+ (liquid and gel). In the presence of Ca2+, the gels were formed in the stoichiometric conditions of the number of moles of positive and negative charges. On the other hand, in the presence of TA-N(CH3)3+, the experimental conditions were different because it is enough that the number of moles of sulfonate groups and positive charges are greater than 2.296 × 10−5 moles and 0.483 × 10−5 moles, respectively.

3.3. Structure of Networks and Antioxidant Properties

The mechanical properties of the PHOSO3−/Ca2+ networks are strongly dependent of the polymer and CaCl2 concentration (Table 1). Dynamic viscoelastic measurement results show that at the higher frequency region G’ is larger than G”, showing that these gels present predominantly elastic properties. The modulus G’ depends on the concentration of CaCl2 and increases linearly with the concentration of PHOSO3−, which shows the influence of hydrophobic interactions between chains and undoubtedly the presence of entanglements. This effect is superimposed on the ionic bonds between the polymer and Ca2+. However, the elastic modulus obtained remains low and does not exceed 40 Pa. Although the network keeps its structure for a week, the addition of water led to the deterioration of the network. The low percentage of SO3− groups (33%) did not allow the formation of enough ionic interactions with Ca2+. The use of other calcium salts such as CaCO3 was studied, but its low solubility in water did not allow the formation of the network, or even CaSO4·2H2O in the presence of Na2HPO4, which is often used as a gelation accelerator [38].
Although the formation of a tannic acid-based network often requires a certain pH value necessary to have the phenolate groups [44,45,46], the advantage of our system is that there is no pH-dependence of the gel formation. In the physiological medium, the tannic acid derivative TA-N(CH3)3+ and the sulfonate PHA always have quaternary amine and sulfonate groups, respectively. The PHOSO3−/TA-N(CH3)3+ network has better mechanical properties than the gel obtained in the presence of Ca2+ (Figure 7). Indeed, the viscoelastic modulus at 100 Hz was much larger than those of the PHOSO3−/Ca2+ network. The elastic modulus of the PHOSO3−/TA-N(CH3)3+ network was stable even after 5 months. This was due to the presence of polyphenolic moieties that gave the network a very high stability and remarkable mechanical properties despite the low proportion of SO3−. Unlike the PHOSO3−/Ca2+ network, the addition of water to the PHOSO3−/TA-N(CH3)3+ network did not disrupt the structure of the network, and the network structure was maintained even after the rheological studies. Moreover, the formation of the network was a completely reversible process even after freeze-drying without any change of the viscoelastic modulus.
The antioxidant capacity was assessed using the DPPH radical scavenging assay. This method consists in performing a reduction of the DPPH radical to its non-radical form in the presence of tannic acid, a hydrogen donating compound (Figure 8). The solution containing DPPH has a purple color, corresponding to a UV-visible absorbance at 517 nm. In the presence of TA, TA-N(CH3)3+, and PHOSO3−/TA-N(CH3)3+, the solutions became yellow and presented significant antiradical activity with a radical scavenging activity (% RSA) superior to 82%.

4. Conclusions

A copolymer based on unsaturated PHAs was functionalized with the polar SO3− sulfonate groups to promote, on the one hand, its solubility in water [26,27], and on the other hand, ionic interactions with cations. An efficient and reproducible method for the synthesis of copolymer of water soluble PHOSO3− was developed by thiol-ene reaction in the presence of sodium-3-mercapto-1-ethanesulfonate. This copolymer was further used for the preparation of network by ions’ interaction with different cations, namely Ca2+, Ba2+, and Mg2+. Among them, only Ca2+ presented the ability to form a gel in the well-defined contents. To reinforce the mechanical properties and stability of the gels, a polycationic derivative of tannic acid was synthesized by reaction with glycidyl trimethyl ammonium chloride (GTMA). The presence of aromatic groups and cationic charges improved the elastic modulus from 40 Pa obtained with Ca2+ to 4200 Pa in the presence of TA-N(CH3)3+. The antioxidant networks based on PHOSO3−/TA-N(CH3)3+ were stable for 5 months in a buffered physiological environment and constitute a new generation of soft biomaterials.

Author Contributions

Conceptualization, L.B., E.R. and V.L.; methodology, L.B., E.R.; investigation, L.B., E.R. and V.L.; writing—original draft preparation, L.B., E.R. and V.L.; supervision, E.R. and V.L. All authors have read and agreed to the published version of the manuscript.

Funding

Financial support from ANR PRCI (SeaBioP Project, France).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Financial support from ANR PRCI (SeaBioP Project, France) is sincerely acknowledged.

Conflicts of Interest

The authors declare no conflict of interest

References

  1. Steinbüchel, A.; Valentin, H.E. Diversity of bacterial polyhydroxyalkanoic acids. FEMS Microbiol. Lett. 1995, 128, 219–228. [Google Scholar] [CrossRef]
  2. Sudesh, K.; Abe, H.; Doi, Y. Synthesis, structure and properties of polyhydroxyalkanoates: Biological polyesters. Prog. Polym. Sci. 2000, 25, 1503–1555. [Google Scholar] [CrossRef]
  3. Lenz, R.W.; Marchessault, R.H. Bacterial Polyesters: Biosynthesis, Biodegradable Plastics and Biotechnology. Biomacromolecules 2005, 6, 1–8. [Google Scholar]
  4. Numata, K.; Abe, H.; Iwata, T. Biodegradability of Poly(hydroxyalkanoate) Materials. Materials 2009, 2, 1104–1126. [Google Scholar] [CrossRef]
  5. Volova, T.G.; Prudnikova, S.V.; Vinogradova, O.N.; Syrvacheva, D.A.; Shishatskaya, E.I. Microbial Degradation of Polyhydroxyalkanoates with Different Chemical Compositions and Their Biodegradability. Microb. Ecol. 2017, 73, 353–367. [Google Scholar] [CrossRef]
  6. Zhang, J.; Shishatskaya, E.I.; Volova, T.G.; Silva, L.F.; Chen, G.-Q. Polyhydroxyalkanoates (PHA) for therapeutic applications. Mater. Sci. Eng. C 2018, 86, 144–150. [Google Scholar] [CrossRef] [Green Version]
  7. Rai, R.; Keshavarz, T.; Roether, J.; Boccaccini, A.R.; Roy, I. Medium chain length polyhydroxyalkanoates, promising new biomedical materials for the future. Mater. Sci. Eng. R Rep. 2011, 72, 29–47. [Google Scholar] [CrossRef]
  8. Koller, M. Biodegradable and Biocompatible Polyhydroxy-alkanoates (PHA): Auspicious Microbial Macromolecules for Pharmaceutical and Therapeutic Applications. Molcules 2018, 23, 362. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  9. Williams, S.F.; Martin, D.P. Applications of Polyhydroxyalkanoates (PHA). Med. Pharm. 2002, 10, 91–121. [Google Scholar]
  10. Bear, M.M.; Renard, E.; Randriamahefa, S.; Langlois, V.; Guérin, P. Preparation of a bacterial polyester with carboxy groups in side chains. C. R. l’Academie. Sci. Ser. IIC Univers. 2001, 4, 289–293. [Google Scholar]
  11. Chen, G.-Q.; Chen, X.-Y.; Wu, F.-Q.; Chen, J.-C. Polyhydroxyalkanoates (PHA) toward cost competitiveness and functionality. Adv. Ind. Eng. Polym. Res. 2020, 3, 1–7. [Google Scholar] [CrossRef]
  12. Renard, E.; Poux, A.; Timbart, L.; Langlois, A.V.; Guérin, P. Preparation of a Novel Artificial Bacterial Polyester Modified with Pendant Hydroxyl Groups. Biomacromolecules 2005, 6, 891–896. [Google Scholar] [CrossRef] [PubMed]
  13. Eroğlu, M.S.; Hazer, B.; Ozturk, T.; Çaykara, T. Hydroxylation of pendant vinyl groups of poly(3-hydroxy undec-10-enoate) in high yield. J. Appl. Polym. Sci. 2005, 97, 2132–2139. [Google Scholar] [CrossRef]
  14. Stigers, J.D.; Tew, G.N. Poly(3-hydroxyalkanoate)s Functionalized with Carboxylic Acid Groups in the Side Chain. Biomacromolecules 2003, 4, 193–195. [Google Scholar] [CrossRef]
  15. Renard, E.; Timbart, L.; Vergnol, G.; Langlois, V. Role of carboxyl pendant groups of medium chain length poly(3-hydroxyalkanoate)s in biomedical temporary applications. J. Appl. Polym. Sci. 2010, 117, 1888–1896. [Google Scholar] [CrossRef]
  16. Park, W.H.; Lenz, R.W.; Goodwin, S. Epoxidation of Bacterial Polyesters with Unsaturated Side Chains. I. Production and Epoxidation of Polyesters from 10-Undecenoic Acid. Macromolecules 1998, 31, 1480–1486. [Google Scholar] [CrossRef]
  17. Hazer, B.; Steinbüchel, A. Increased diversification of polyhydroxyalkanoates by modification reactions for industrial and medical applications. Appl. Microbiol. Biotechnol. 2007, 74, 1–12. [Google Scholar] [CrossRef]
  18. Domenek, S.; Langlois, V.; Renard, E. Bacterial polyesters grafted with poly(ethylene glycol): Behaviour in aqueous media. Polym. Degrad. Stab. 2007, 92, 1384–1392. [Google Scholar] [CrossRef]
  19. Renard, E.; Tanguy, P.-Y.; Samain, E.; Guérin, P. Synthesis of novel graft polyhydroxyalkanoates. Macromol. Symp. 2003, 197, 11–18. [Google Scholar] [CrossRef]
  20. Renard, E.; Ternat, C.; Langlois, V.; Guérin, P. Synthesis of Graft Bacterial Polyesters for Nanoparticles Preparation. Macromol. Biosci. 2003, 3, 248–252. [Google Scholar] [CrossRef]
  21. Babinot, J.; Renard, E.; Langlois, V. Preparation of Clickable Poly(3-hydroxyalkanoate) (PHA): Application to Poly(ethylene glycol) (PEG) Graft Copolymers Synthesis. Macromol. Rapid Commun. 2010, 31, 619–624. [Google Scholar] [CrossRef] [PubMed]
  22. Babinot, J.; Renard, E.; Le Droumaguet, B.; Guigner, J.-M.; Mura, S.; Nicolas, J.; Couvreur, P.; Langlois, V.; Patrick, C. Facile Synthesis of Multicompartment Micelles Based on Biocompatible Poly(3-hydroxyalkanoate). Macromol. Rapid Commun. 2012, 34, 362–368. [Google Scholar] [CrossRef] [PubMed]
  23. Babinot, J.; Renard, E.; Langlois, V. Controlled Synthesis of Well Defined Poly(3-hydroxyalkanoate)s-based Amphiphilic Diblock Copolymers Using Click Chemistry. Macromol. Chem. Phys. 2010, 212, 278–285. [Google Scholar] [CrossRef]
  24. Babinot, J.; Guigner, J.-M.; Renard, E.; Langlois, V. Poly(3-hydroxyalkanoate)-derived amphiphilic graft copolymers for the design of polymersomes. Chem. Commun. 2012, 48, 5364–5366. [Google Scholar] [CrossRef] [PubMed]
  25. Sparks, J.; Scholz, C. Synthesis and Characterization of a Cationic Poly(β-hydroxyalkanoate). Biomacromolecules 2008, 9, 2091–2096. [Google Scholar] [CrossRef]
  26. Modjinou, T.; Lemechko, P.; Babinot, J.; Versace, D.L.; Langlois, V.; Renard, E. Poly(3-hydroxyalkanoate) sulfonate: From nanopartices toward water soluble polyesters. Eur. Polym. J. 2015, 68, 471–479. [Google Scholar]
  27. Jain-Beuguel, C.; Li, X.; Renault, L.H.; Modjinou, T.; Colin, C.S.; Gref, R.; Renard, E.; Langlois, V. Water-Soluble Poly(3-hydroxyalkanoate) Sulfonate: Versatile Biomaterials Used as Coatings for Highly Porous Nano-Metal Organic Framework. Biomacromolecules 2019, 20, 3324–3332. [Google Scholar] [CrossRef]
  28. Chung, C.W.; Kim, H.W.; Kim, Y.B.; Rhee, Y.H. Poly(ethylene glycol)-grafted poly(3-hydroxyundecenoate) networks for enhanced blood compatibility. Int. J. Biol. Macromol. 2003, 32, 17–22. [Google Scholar] [CrossRef]
  29. Jiang, L.; Luo, Z.; Loh, X.J.; Wu, Y.-L.; Li, Z. PHA-Based Thermogel as a Controlled Zero-Order Chemotherapeutic Delivery System for the Effective Treatment of Melanoma. ACS Appl. Bio Mater. 2019, 2, 3591–3600. [Google Scholar] [CrossRef]
  30. Le Fer, G.; Babinot, J.; Versace, D.-L.; Langlois, V.; Renard, E. An Efficient Thiol-Ene Chemistry for the Preparation of Amphiphilic PHA-Based Graft Copolymers. Macromol. Rapid Commun. 2012, 33, 2041–2045. [Google Scholar] [CrossRef]
  31. Hao, J.; Deng, X. Semi-interpenetrating networks of bacterial poly(3-hydroxybutyrate) with net-poly(ethylene glycol). Polymer 2001, 42, 4091–4097. [Google Scholar] [CrossRef]
  32. Zhang, X.; Li, Z.; Che, X.; Yu, L.; Jia, W.; Shen, R.; Chen, J.; Ma, Y.; Chen, G.Q. Synthesis and Characterization of Polyhydroxyalkanoate Organo/Hydrogels. Biomacromolecules 2019, 20, 3303–3312. [Google Scholar] [CrossRef] [PubMed]
  33. Pavon-Djavid, G.; Gamble, L.J.; Ciobanu, M.; Gueguen, V.; Castner, D.G.; Migonney, V. Bioactive Poly(ethylene terephthalate) Fibers and Fabrics: Grafting, Chemical Characterization, and Biological Assessment. Biomacromolecules 2007, 8, 3317–3325. [Google Scholar] [CrossRef] [PubMed]
  34. Silver, J.H.; Hart, A.P.; Williams, E.C.; Cooper, S.L.; Charef, S.; Labarre, D.; Jozefowicz, M. Anticoagulant effects of sulphonated polyurethanes. Biomaterials 1992, 13, 339–344. [Google Scholar] [CrossRef]
  35. Palarasah, Y.; Skjoedt, M.O.; Vitved, L.; Koch, C. Sodium Polyanethole Sulfonate as an Inhibitor of Activation of Complement Function in Blood Culture Systems. J. Clin. Microbiol. 2010, 48, 908–914. [Google Scholar] [CrossRef] [Green Version]
  36. Meder, F.; Brandes, C.; Treccani, L.; Rezwan, K. Controlling protein–particle adsorption by surface tailoring colloidal alumina particles with sulfonate groups. Acta Biomater. 2013, 9, 5780–5787. [Google Scholar] [CrossRef]
  37. Li, G.; Zhang, G.; Sun, R.; Wong, C.-P. Mechanical strengthened alginate/polyacrylamide hydrogel crosslinked by barium and ferric dual ions. J. Mater. Sci. 2017, 52, 8538–8545. [Google Scholar] [CrossRef]
  38. Larsen, B.E.; Bjørnstad, J.; Pettersen, E.O.; Tønnesen, H.H.; Melvik, J.E. Rheological characterization of an injectable alginate gel system. BMC Biotechnol. 2015, 15, 29. [Google Scholar] [CrossRef] [Green Version]
  39. Espona-Noguera, A.; Ciriza, J.; Cañibano-Hernández, A.; Fernandez, L.; Ochoa, I.; Saenz del Burgo, L.; Pedraz, J.L. Tunable injectable alginate-based hydrogel for cell therapy in Type 1 Diabetes Mellitus. Int. J. Biol. Macromol. 2018, 107, 1261–1269. [Google Scholar]
  40. Badhani, B.; Sharma, N.; Kakkar, R. Gallic acid: A versatile antioxidant with promising therapeutic and industrial applications. RSC Adv. 2015, 5, 27540–27557. [Google Scholar] [CrossRef]
  41. Zahrani, N.A.A.L.; El-Shishtawy, R.M.; Asiri, A.M. Recent developments of gallic acid derivatives and their hybrids in medicinal chemistry: A review European. J. Med. Chem. 2020, 204, 112609–112646. [Google Scholar] [CrossRef] [PubMed]
  42. Glaive, A.-S.; Modjinou, T.; Versace, D.-L.; Abbad-Andaloussi, S.; Dubot, P.; Langlois, V.; Renard, E. Design of Antibacterial and Sustainable Antioxidant Networks Based on Plant Phenolic Derivatives Used As Delivery System of Carvacrol or Tannic Acid. ACS Sustain. Chem. Eng. 2017, 5, 2320–2329. [Google Scholar] [CrossRef]
  43. Bhone, K.; Lim, M.; Sing, C.; Wei, Z. Tannic Acid as Phytochemical Potentiator for Antibiotic Resistance Adaptation. APCBEE Procedia 2013, 7, 175–181. [Google Scholar]
  44. Xie, Y.; Chen, S.; Zhang, X.; Shi, Z.; Wei, Z.; Bao, J.; Zhao, W.; Zhao, C. Engineering of Tannic Acid Inspired Antifouling and Antibacterial Membranes through Co-deposition of Zwitterionic Polymers and Ag Nanoparticles. Ind. Eng. Chem. Res. 2019, 58, 11689–11697. [Google Scholar] [CrossRef]
  45. Fan, H.; Wang, L.; Feng, X.; Bu, Y.; Wu, D.; Jin, Z. Supramolecular Hydrogel Formation Based on Tannic Acid. Macromolecules 2017, 50, 666–676. [Google Scholar] [CrossRef]
  46. Fan, H.; Wang, J.; Zhang, Q.; Jin, Z. Tannic Acid-Based Multifunctional Hydrogels with Facile Adjustable Adhesion and Cohesion Contributed by Polyphenol Supramolecular Chemistry. ACS Omega 2017, 2, 6668–6676. [Google Scholar] [CrossRef]
  47. Zheng, L.-Y.; Shi, J.-M.; Chi, Y.-H. Tannic Acid Physically Cross-Linked Responsive Hydrogel. Macromol. Chem. Phys. 2018, 219. [Google Scholar] [CrossRef]
  48. Guo, J.; Sun, W.; Kim, J.P.; Lu, X.; Li, Q.; Lin, M.; Mrowczynski, O.; Rizk, E.B.; Cheng, J.; Qian, G.-Y.; et al. Development of tannin-inspired antimicrobial bioadhesives. Acta Biomater. 2018, 72, 35–44. [Google Scholar] [CrossRef]
  49. Park, K.; Jeong, H.; Tanum, J.; Yoo, J.-C.; Hong, J. Developing regulatory property of gelatin-tannic acid multilayer films for coating-based nitric oxide gas delivery system. Sci. Rep. 2019, 9, 1–8. [Google Scholar] [CrossRef] [Green Version]
  50. Liu, R.; Zheng, J.; Guo, R.; Luo, J.; Yuan, Y.; Liu, X. Synthesis of New Biobased Antibacterial Methacrylates Derived from Tannic Acid and Their Application in UV-Cured Coatings. Ind. Eng. Chem. Res. 2014, 53, 10835–10840. [Google Scholar] [CrossRef]
  51. Assifaoui, A.; Lerbret, A.; Huynh, U.T.D.; Neiers, F.; Chambin, O.; Loupiac, C.; Cousin, F.; Uyen, H.T.D. Structural behaviour differences in low methoxy pectin solutions in the presence of divalent cations (Ca 2+ and Zn 2+): A process driven by the binding mechanism of the cation with the galacturonate unit. Soft Matter 2015, 11, 551–560. [Google Scholar] [CrossRef] [PubMed]
  52. Huynh, U.T.D.; Lerbret, A.; Neiers, F.; Chambin, O.; Assifaoui, A. Binding of Divalent Cations to Polygalacturonate: A mechanism Drien by the Hydration Water. J. Phys. Chem. 2016, 120, 1021–1032. [Google Scholar] [CrossRef] [PubMed]
Bioengineering 08 00009 g001 550
Figure 1. Gelation process of PHOSO3− induced by cationic species as Ca2+, Mg2+, Ba2+, and gallic and tannic acid derivatives.
Figure 1. Gelation process of PHOSO3− induced by cationic species as Ca2+, Mg2+, Ba2+, and gallic and tannic acid derivatives.
Bioengineering 08 00009 g001
Bioengineering 08 00009 g002 550
Figure 2. 1H NMR spectra: (a) PHOU in CDCl3; (b) PHOSO3− in dimethyl sulfoxide, DMSO-d6.
Figure 2. 1H NMR spectra: (a) PHOU in CDCl3; (b) PHOSO3− in dimethyl sulfoxide, DMSO-d6.
Bioengineering 08 00009 g002
Bioengineering 08 00009 g003 550
Figure 3. Schematic representation of TA-N(CH3)3+ by chemical modification of tannic acid in the presence of GTMA.
Figure 3. Schematic representation of TA-N(CH3)3+ by chemical modification of tannic acid in the presence of GTMA.
Bioengineering 08 00009 g003
Bioengineering 08 00009 g004 550
Figure 4. 1H NMR spectra of (a) tannic acid in DMSO, (b) GTMA in D2O, (c) TA- N(CH3)3+ in D2O, and (d) GA-N(CH3)3+ in D2O.
Figure 4. 1H NMR spectra of (a) tannic acid in DMSO, (b) GTMA in D2O, (c) TA- N(CH3)3+ in D2O, and (d) GA-N(CH3)3+ in D2O.
Bioengineering 08 00009 g004
Bioengineering 08 00009 g005 550
Figure 5. Effect of the cationic species on the network formation with a PHOSO3− (concentration of 27 g·L−1).
Figure 5. Effect of the cationic species on the network formation with a PHOSO3− (concentration of 27 g·L−1).
Bioengineering 08 00009 g005
Bioengineering 08 00009 g006 550
Figure 6. Schematic representation of the effect of the number of positive charges for Ca2+ (A) or TA-N(CH3)3+ (B) as a function of the amount of SO3− in the gel formation.
Figure 6. Schematic representation of the effect of the number of positive charges for Ca2+ (A) or TA-N(CH3)3+ (B) as a function of the amount of SO3− in the gel formation.
Bioengineering 08 00009 g006
Bioengineering 08 00009 g007 550
Figure 7. Frequency dependences of the storage modulus G’ and loss modulus G’’ of PHOSO3− at 96 g·L−1 with CaCl2 and TA-N(CH3)3+.
Figure 7. Frequency dependences of the storage modulus G’ and loss modulus G’’ of PHOSO3− at 96 g·L−1 with CaCl2 and TA-N(CH3)3+.
Bioengineering 08 00009 g007
Bioengineering 08 00009 g008 550
Figure 8. Absorption UV spectra in the presence of DPPH (A) and reduced DPPH after reaction with TA (B), TA-N(CH3)3+ (C), and PHOSO3−/TA-N(CH3)3+ (D).
Figure 8. Absorption UV spectra in the presence of DPPH (A) and reduced DPPH after reaction with TA (B), TA-N(CH3)3+ (C), and PHOSO3−/TA-N(CH3)3+ (D).
Bioengineering 08 00009 g008
Table
Table 1. Influence of PHO-SO3− concentration on gel mechanical properties of PHOSO3−/Ca2+ networks at 10 Hz.
Table 1. Influence of PHO-SO3− concentration on gel mechanical properties of PHOSO3−/Ca2+ networks at 10 Hz.
[PHO-SO3−] (g/L)nSO3− ×105nCa2+ ×105n Positive Charges ×105G’ (Pa)G” (Pa)
471.931.42.84.013.93
592.421.53.014.6211.26
682.791.42.824.2012.78
712.911.83.638.3824.92
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Brelle, L.; Renard, E.; Langlois, V. Antioxidant Network Based on Sulfonated Polyhydroxyalkanoate and Tannic Acid Derivative. Bioengineering 2021, 8, 9. https://doi.org/10.3390/bioengineering8010009

AMA Style

Brelle L, Renard E, Langlois V. Antioxidant Network Based on Sulfonated Polyhydroxyalkanoate and Tannic Acid Derivative. Bioengineering. 2021; 8(1):9. https://doi.org/10.3390/bioengineering8010009

Chicago/Turabian Style

Brelle, Laura, Estelle Renard, and Valerie Langlois. 2021. "Antioxidant Network Based on Sulfonated Polyhydroxyalkanoate and Tannic Acid Derivative" Bioengineering 8, no. 1: 9. https://doi.org/10.3390/bioengineering8010009

APA Style

Brelle, L., Renard, E., & Langlois, V. (2021). Antioxidant Network Based on Sulfonated Polyhydroxyalkanoate and Tannic Acid Derivative. Bioengineering, 8(1), 9. https://doi.org/10.3390/bioengineering8010009

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop