Biomaterials Translational ›› 2022, Vol. 3 ›› Issue (4): 250-263.doi: 10.12336/biomatertransl.2022.04.005
• REVIEW • Previous Articles Next Articles
Jingyu Fan1, Elizabeth Pung1, Yuan Lin2, Qian Wang1,*()
Received:
2022-11-09
Revised:
2022-12-09
Accepted:
2022-12-20
Online:
2022-12-29
Published:
2022-12-28
Contact:
Qian Wang
E-mail:Wang263@mailbox.sc.edu
About author:
Qian Wang,Wang263@mailbox.sc.edu.
Fan, J.; Pung, E.; Lin, Y.; Wang, Q. Recent development of hydrogen sulfide-releasing biomaterials as novel therapies: a narrative review. Biomater Transl. 2022, 3(4), 250-263.
Figure 1. Biosynthesis and catabolism of H2S. In mammals, H2S is produced endogenously from cysteine, serine, homocysteine, and other substrates primarily through the actions of three major enzymes. CBS is mainly localized in the nervous system, brain and liver; CSE is mainly localized in the cardiovascular system to produce H2S; MST is predominantly localized in mitochondria. In addition, the activities of gut microbiota, glycolysis and phosphogluconate of glucose, the GSH and “sulfane sulfur” pools may also contribute to the maintenance of H2S concentrations in plasma and tissue.11,28?-30 CAT: cystine aminotransferase; CBS: cystathionine–β–synthase; CSE: cystathionine–γ–lyase; GSH; glutathione; H2S: hydrogen sulfide; MST: mercaptopyruvate sulfurtransferase.
Figure 2. Donor compounds for H2S release. Recent advances in the development of H2S donors has revealed multiple types of donors, namely, pH–sensitive donors including JK1 and GYY 4137,43–45 enzyme–activated donors such as BW–HP–101,46–48 reactive–oxygen species such as PeroxyTCMs,49 and thiol–triggered donors including TAGDDs and SATO.50,51 H2S: hydrogen sulfide; TAGDD: thiol–activated gem–dithiol–based H2S donor; SATO: S–aroylthiooxime; PeroxyTCM: PeroxyThioCarbaMate.
Figure 3. Physical incorporation of H2S donor into biomaterials. (A) H2S–release fibres by incorporating thiol–dependent H2S donor, NSHD–1, in the electrospun PCL–fibres: SEM images of H2S–fibres (a–c) and PCL–fibres (d–f). All images share the same scale bar (5 μm) in f. (g) The H2S donor, NSHD–1, can release H2S in the presence of cysteine or GSH. (h) Fibre diameters plot as a function of solution concentrations. The dopant, NSHD1, has no obvious effect on fibre diameters.65 (B) H2S–releasing sponge sodium alginate/JK–1 by incorporating the pH–dependent H2S donor JK–1 into an alginate sponge obtained by crosslinking sodium alginate with Ca2+.57 Reprinted from Feng et al.65 and Zhao et al.57 Copyright 2015 and 2020, with permission from Elsevier Ltd. GSH: glutathione; NSHD–1: N–(benzoylthio) benzamide; PCL: polycaprolactone; SEM: scanning electron microscope.
Figure 4. H2S donor units covalently linked to material backbones. (A) H2S–releasing SATO–unit was incorporated to the polymer, which could be self–assembled into spherical micelles with an average diameter of 21 ± 2 nm. Reprinted from Foster et al.72 (B) Three isomeric peptide?H2S donor conjugates assembled into twisted ribbons and nanocoils in aqueous solution. Reprinted from Wang et al.74 AIBN: 2,2′–azobis(2–methylpropionitrile; DMF: dimethylformamide; FBEMA: 2–(4–formylbenzoyloxy)ethyl methacrylate; H2S: hydrogen sulfide; rt: room temperature; SATO: S–aroylthiooxime; SEM: scanning electron microscope; TFA: trifluoroacetic acid.
Figure 5. H2S donors act in cardiovascular disease. (A) JK1 gives rise to faster H2S release under acidic condition, of which is distinctive feature of ischemia microenvironment compared to normal physiological condition. Reprinted with permission from Kang et al.45 Copyright ? 2016 American Chemical Society. (B) H2S donor micelles protect cardiomyocytes from ischemic cell death. (B1) Chemical structure of ADT–OH. (B2) A block copolymer having ADT–groups (PAM–PADT) forms ADT micelles by self–assembly. (B3) Intracellular release of H2S from ADT micelles prevents apoptotic damage of cardiomyocytes under ischemic condition. Reprinted with permission from Takatani–Nakase et al.85 Copyright ? Royal Society of Chemistry 2017. ADT: anethole dithiolethione; ADT–OH: 5–(4–hydroxyphenyl)–3H–1,2–dithiole–3–thione; H2S: hydrogen sulfide; PAM–PADT: poly (N–acryloy morpholine)–poly anethole dithiolethione.
Figure 6. Schematic illustrating the preparation of injectable HA–JK1 hydrogel and its application to full–thickness dermal wound. (Left) JK1, as H2S donor, was incorporated in the HA based injectable hydrogel, which can be used in the mouse wonder model system. (Right) The local low pH condition near the wound could promoted the fast release of H2S of JK1, which could effectively accelerate the wound healing through promoting cell proliferation, angiogenesis and more importantly, suppressing inflammation via inducing M2 macrophage polarization. Reprinted from Wu et al.56 Copyright 2019, with permission from Elsevier Ltd. H2S: hydrogen sulfide; HA: hyaluronic acid; IL: interleukin; TNF–α: tumour necrosis factor–α.
Application | H2S donor/biomaterials | Research model | Effects/outcome | Proposed mechanism | Reference |
---|---|---|---|---|---|
Cardioprotection | NaHS | Murine infarction model | Infarcted size and mortality significantly decreased | Upregulation of Bcl–2, demoted expression of Bax, IL–1β and Caspase 3 | |
JKs | H9C2 cardiomyoblasts & murine ischemia/reperfusion model | A dose–dependent | |||
inhibition in cell viability; significantly reduced AAR/LV and INS/AAR | |||||
S–diclofenac | Rabbit model | Improved reperfusion pressure, anti–ischemic activity, activation of KATP channel | |||
DAT–MSN | Cardiomyocyte, murine infarction model | inhibited myocardial inflammation, greater reduction in the infarct | Same as above | ||
area and preserved cardiac ejection fraction | |||||
GYY4137 | Cardiomyocyte, murine infarction | Infarcted size reduced, improved cardiac functions | Same as above | ||
ADT–OH/PAM–PADT micelles | Rat cardiomyocytes | Rescue cells from apoptosis | |||
PHDCs/SATO | H9C2 cardiomyoblasts | Mitigated Dox–induced toxicity | |||
ALG–CHO/APTC/ADSC | ADSC/rat model | Improved heart function | Suppressed TNF–α, upregulation of genes related to angiogenesis and cardiac function | ||
PFHy–MBs/CST | hCPCs | Improved cell growth | |||
Atherosclerosis | NaHS | Apolipoprotein–E K.O. mice model & HUVEC | Antiatherogenic effect with promoted cell viability | Inhibited ICAM–1 and TNF–α signalling | |
APA/SATO | HUVEC | Improved cell proliferation and migration | |||
Chitosan/HA hydrogel/ACS14 | Platelet, rat model | Reduced inflammatory and AS lesion | |||
Pulmonary arterial hypertension | LPM/ACS14 | PAH rat model, HPAEC | Delayed and reversed progression of PAH | Suppressed NF–κB–Snail pathway | |
Wound healing | NaHS | HaCaT cell model, human epidermal melanocytes, HUVEC diabetic mice model | Promoted viability and differentiation | Promoted proliferation and differentiation via ATG5, TRP–1 signalling, angiogenesis via ANG–1, anti–inflammatory effect suppressing IL–6, TNF–α and MMP–9 | |
Na2S | HUVEC, diabetic mice model | Suppressed inflammation, promoted migration and proliferation | Upregulation of KATP/P38/ERK/MAPK/VEGF signalling, and VEGFR2 transcription | ||
NSHD1/PCL fibre | NIH 3T3, H9C2 cell model | Significantly prolonged release time, decreased ROS production | |||
JK1/PCL fibre | NIH 3T3, mice model | Enhanced wound regeneration, prolonged release time | |||
JK1/HA hydrogel | Mice model | Fast wound healing with enhanced cell proliferation and angiogenesis | Macrophage polarization towards M2 phenotype, suppressed TNF–α | ||
JK1/SA hydrogel | L929 cell, rat model | Enhanced wound healing, promoted release profile | |||
H2S/SA hydrogel | L929 cell, rat model | Promoted wound healing in a dose dependent manner | |||
NaHS/rMaSp fibre | NIH 3T3, mice model | Promoted wound healing with EPC | |||
SATO/PCL fibre | NHEK cells, diabetic mice model | Bacterial inhibition, promoted diabetic wound healing | |||
Anti–bacterial | SATO/APA biofilm/dipeptides | Staphylococcus aureus | Inhibited bacterial growth | ||
Intervertebral disc degeneration | JK1/Col hydrogel | Rat model, NP cell | Inhibited inflammatory process and cell apoptosis | Suppressing TNF–α, NF–κB, IL–1β expression and deactivation of P65 signalling | |
Tissue engineering | GaOS/PLA membrane | Cardiac mesenchymal stem cell | Promoted proliferation with reduced oxidative damage | ||
GYY4137/fibroin scaffold | Mouse fibroblast, hBMSC | Enhanced cell viability | |||
Anti–cancer | Trisulfide/PEG–cholesteryl | MCF7 breast cancer cell | Suppressed tumourigenesis | Normalization of COL–1 expression | |
ADT/AML | HepG2 cell, mice xenograft model | Reduction of tumour size, facilitate magnetic resonance imaging |
Table 1. Summary of applications of H2S donors and H2S–releasing biomaterials
Application | H2S donor/biomaterials | Research model | Effects/outcome | Proposed mechanism | Reference |
---|---|---|---|---|---|
Cardioprotection | NaHS | Murine infarction model | Infarcted size and mortality significantly decreased | Upregulation of Bcl–2, demoted expression of Bax, IL–1β and Caspase 3 | |
JKs | H9C2 cardiomyoblasts & murine ischemia/reperfusion model | A dose–dependent | |||
inhibition in cell viability; significantly reduced AAR/LV and INS/AAR | |||||
S–diclofenac | Rabbit model | Improved reperfusion pressure, anti–ischemic activity, activation of KATP channel | |||
DAT–MSN | Cardiomyocyte, murine infarction model | inhibited myocardial inflammation, greater reduction in the infarct | Same as above | ||
area and preserved cardiac ejection fraction | |||||
GYY4137 | Cardiomyocyte, murine infarction | Infarcted size reduced, improved cardiac functions | Same as above | ||
ADT–OH/PAM–PADT micelles | Rat cardiomyocytes | Rescue cells from apoptosis | |||
PHDCs/SATO | H9C2 cardiomyoblasts | Mitigated Dox–induced toxicity | |||
ALG–CHO/APTC/ADSC | ADSC/rat model | Improved heart function | Suppressed TNF–α, upregulation of genes related to angiogenesis and cardiac function | ||
PFHy–MBs/CST | hCPCs | Improved cell growth | |||
Atherosclerosis | NaHS | Apolipoprotein–E K.O. mice model & HUVEC | Antiatherogenic effect with promoted cell viability | Inhibited ICAM–1 and TNF–α signalling | |
APA/SATO | HUVEC | Improved cell proliferation and migration | |||
Chitosan/HA hydrogel/ACS14 | Platelet, rat model | Reduced inflammatory and AS lesion | |||
Pulmonary arterial hypertension | LPM/ACS14 | PAH rat model, HPAEC | Delayed and reversed progression of PAH | Suppressed NF–κB–Snail pathway | |
Wound healing | NaHS | HaCaT cell model, human epidermal melanocytes, HUVEC diabetic mice model | Promoted viability and differentiation | Promoted proliferation and differentiation via ATG5, TRP–1 signalling, angiogenesis via ANG–1, anti–inflammatory effect suppressing IL–6, TNF–α and MMP–9 | |
Na2S | HUVEC, diabetic mice model | Suppressed inflammation, promoted migration and proliferation | Upregulation of KATP/P38/ERK/MAPK/VEGF signalling, and VEGFR2 transcription | ||
NSHD1/PCL fibre | NIH 3T3, H9C2 cell model | Significantly prolonged release time, decreased ROS production | |||
JK1/PCL fibre | NIH 3T3, mice model | Enhanced wound regeneration, prolonged release time | |||
JK1/HA hydrogel | Mice model | Fast wound healing with enhanced cell proliferation and angiogenesis | Macrophage polarization towards M2 phenotype, suppressed TNF–α | ||
JK1/SA hydrogel | L929 cell, rat model | Enhanced wound healing, promoted release profile | |||
H2S/SA hydrogel | L929 cell, rat model | Promoted wound healing in a dose dependent manner | |||
NaHS/rMaSp fibre | NIH 3T3, mice model | Promoted wound healing with EPC | |||
SATO/PCL fibre | NHEK cells, diabetic mice model | Bacterial inhibition, promoted diabetic wound healing | |||
Anti–bacterial | SATO/APA biofilm/dipeptides | Staphylococcus aureus | Inhibited bacterial growth | ||
Intervertebral disc degeneration | JK1/Col hydrogel | Rat model, NP cell | Inhibited inflammatory process and cell apoptosis | Suppressing TNF–α, NF–κB, IL–1β expression and deactivation of P65 signalling | |
Tissue engineering | GaOS/PLA membrane | Cardiac mesenchymal stem cell | Promoted proliferation with reduced oxidative damage | ||
GYY4137/fibroin scaffold | Mouse fibroblast, hBMSC | Enhanced cell viability | |||
Anti–cancer | Trisulfide/PEG–cholesteryl | MCF7 breast cancer cell | Suppressed tumourigenesis | Normalization of COL–1 expression | |
ADT/AML | HepG2 cell, mice xenograft model | Reduction of tumour size, facilitate magnetic resonance imaging |
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