Recent development of hydrogen sulfide-releasing biomaterials as novel therapies:a narrative review

doi:10.12336/biomatertransl.2022.04.005

Biomaterials Translational ›› 2022, Vol. 3 ›› Issue (4): 250-263.doi: 10.12336/biomatertransl.2022.04.005

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Recent development of hydrogen sulfide-releasing biomaterials as novel therapies:a narrative review

Jingyu Fan¹, Elizabeth Pung¹, Yuan Lin², Qian Wang¹^,^*()

1 Department of Chemistry and Biochemistry, University of South Carolina, Columbia, SC, USA
2 State Key Laboratory of Polymer Physics and Chemistry, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun, Jilin Province, China

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.

Abstract

Abstract:

Hydrogen sulfide (H₂S) has been reported as an endogenous gasotransmitter that contributes to the modulation of a myriad of biological signalling pathways, which includes maintaining homeostasis in living organisms at physiological concentrations, controlling protein sulfhydration and persulfidation for signalling processes, mediating neurodegeneration, and regulating inflammation and innate immunity, etc. As a result, researchers are actively exploring effective approaches to evaluate the properties and the distribution of H₂S in vivo. Furthermore, the regulation of the physiological conditions of H₂S in vivo introduces the opportunity to further study the molecular mechanisms by which H₂S regulates cellular functions. In recent years, many H₂S–releasing compounds and biomaterials that can deliver H₂S to various body systems have been developed to provide sustained and stable H₂S delivery. Additionally, various designs of these H₂S–releasing biomaterials have been proposed to aid in the normal conduction of physiological processes, such as cardioprotection and wound healing, by modulating different signalling pathways and cell functionalities. Using biomaterials as a platform to control the delivery of H₂S introduces the opportunity to fine tune the physiological concentration of H₂S in vivo, a key to many therapeutic applications. In this review, we highlight recent research works concerning the development and application of H₂S–releasing biomaterials with a special emphasis to different release triggering conditions in in vivo studies. We believe that the further exploration of the molecular mechanisms underlying H₂S donors and their function when incorporated with various biomaterials will potentially help us understand the pathophysiological mechanisms of different diseases and assist the development of H₂S–based therapies.

Key words: biomaterials, cardiovascular disease, H₂S donors, hydrogen sulfide, wound healing

Cite this article

Figures/Tables 7

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.

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	80?–82, 84
	JKs	H9C2 cardiomyoblasts & murine ischemia/reperfusion model	A dose–dependent		45
			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		83
	DAT–MSN	Cardiomyocyte, murine infarction model	inhibited myocardial inflammation, greater reduction in the infarct	Same as above	84
			area and preserved cardiac ejection fraction
	GYY4137	Cardiomyocyte, murine infarction	Infarcted size reduced, improved cardiac functions	Same as above	84
	ADT–OH/PAM–PADT micelles	Rat cardiomyocytes	Rescue cells from apoptosis		85
	PHDCs/SATO	H9C2 cardiomyoblasts	Mitigated Dox–induced toxicity		91
	ALG–CHO/APTC/ADSC	ADSC/rat model	Improved heart function	Suppressed TNF–α, upregulation of genes related to angiogenesis and cardiac function	93
	PFHy–MBs/CST	hCPCs	Improved cell growth		94
Atherosclerosis	NaHS	Apolipoprotein–E K.O. mice model & HUVEC	Antiatherogenic effect with promoted cell viability	Inhibited ICAM–1 and TNF–α signalling	86, 89
	APA/SATO	HUVEC	Improved cell proliferation and migration		75, 76
	Chitosan/HA hydrogel/ACS14	Platelet, rat model	Reduced inflammatory and AS lesion		92
Pulmonary arterial hypertension	LPM/ACS14	PAH rat model, HPAEC	Delayed and reversed progression of PAH	Suppressed NF–κB–Snail pathway	90
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	102??–105
	Na2S	HUVEC, diabetic mice model	Suppressed inflammation, promoted migration and proliferation	Upregulation of KATP/P38/ERK/MAPK/VEGF signalling, and VEGFR2 transcription	106, 108
	NSHD1/PCL fibre	NIH 3T3, H9C2 cell model	Significantly prolonged release time, decreased ROS production		65
	JK1/PCL fibre	NIH 3T3, mice model	Enhanced wound regeneration, prolonged release time		52
	JK1/HA hydrogel	Mice model	Fast wound healing with enhanced cell proliferation and angiogenesis	Macrophage polarization towards M2 phenotype, suppressed TNF–α	56
	JK1/SA hydrogel	L929 cell, rat model	Enhanced wound healing, promoted release profile		57
	H₂S/SA hydrogel	L929 cell, rat model	Promoted wound healing in a dose dependent manner		115
	NaHS/rMaSp fibre	NIH 3T3, mice model	Promoted wound healing with EPC		116
	SATO/PCL fibre	NHEK cells, diabetic mice model	Bacterial inhibition, promoted diabetic wound healing		117
Anti–bacterial	SATO/APA biofilm/dipeptides	Staphylococcus aureus	Inhibited bacterial growth		118
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	119
Tissue engineering	GaOS/PLA membrane	Cardiac mesenchymal stem cell	Promoted proliferation with reduced oxidative damage		120
	GYY4137/fibroin scaffold	Mouse fibroblast, hBMSC	Enhanced cell viability		121
Anti–cancer	Trisulfide/PEG–cholesteryl	MCF7 breast cancer cell	Suppressed tumourigenesis	Normalization of COL–1 expression	125
	ADT/AML	HepG2 cell, mice xenograft model	Reduction of tumour size, facilitate magnetic resonance imaging		126

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	80?–82, 84
	JKs	H9C2 cardiomyoblasts & murine ischemia/reperfusion model	A dose–dependent		45
			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		83
	DAT–MSN	Cardiomyocyte, murine infarction model	inhibited myocardial inflammation, greater reduction in the infarct	Same as above	84
			area and preserved cardiac ejection fraction
	GYY4137	Cardiomyocyte, murine infarction	Infarcted size reduced, improved cardiac functions	Same as above	84
	ADT–OH/PAM–PADT micelles	Rat cardiomyocytes	Rescue cells from apoptosis		85
	PHDCs/SATO	H9C2 cardiomyoblasts	Mitigated Dox–induced toxicity		91
	ALG–CHO/APTC/ADSC	ADSC/rat model	Improved heart function	Suppressed TNF–α, upregulation of genes related to angiogenesis and cardiac function	93
	PFHy–MBs/CST	hCPCs	Improved cell growth		94
Atherosclerosis	NaHS	Apolipoprotein–E K.O. mice model & HUVEC	Antiatherogenic effect with promoted cell viability	Inhibited ICAM–1 and TNF–α signalling	86, 89
	APA/SATO	HUVEC	Improved cell proliferation and migration		75, 76
	Chitosan/HA hydrogel/ACS14	Platelet, rat model	Reduced inflammatory and AS lesion		92
Pulmonary arterial hypertension	LPM/ACS14	PAH rat model, HPAEC	Delayed and reversed progression of PAH	Suppressed NF–κB–Snail pathway	90
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	102??–105
	Na2S	HUVEC, diabetic mice model	Suppressed inflammation, promoted migration and proliferation	Upregulation of KATP/P38/ERK/MAPK/VEGF signalling, and VEGFR2 transcription	106, 108
	NSHD1/PCL fibre	NIH 3T3, H9C2 cell model	Significantly prolonged release time, decreased ROS production		65
	JK1/PCL fibre	NIH 3T3, mice model	Enhanced wound regeneration, prolonged release time		52
	JK1/HA hydrogel	Mice model	Fast wound healing with enhanced cell proliferation and angiogenesis	Macrophage polarization towards M2 phenotype, suppressed TNF–α	56
	JK1/SA hydrogel	L929 cell, rat model	Enhanced wound healing, promoted release profile		57
	H₂S/SA hydrogel	L929 cell, rat model	Promoted wound healing in a dose dependent manner		115
	NaHS/rMaSp fibre	NIH 3T3, mice model	Promoted wound healing with EPC		116
	SATO/PCL fibre	NHEK cells, diabetic mice model	Bacterial inhibition, promoted diabetic wound healing		117
Anti–bacterial	SATO/APA biofilm/dipeptides	Staphylococcus aureus	Inhibited bacterial growth		118
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	119
Tissue engineering	GaOS/PLA membrane	Cardiac mesenchymal stem cell	Promoted proliferation with reduced oxidative damage		120
	GYY4137/fibroin scaffold	Mouse fibroblast, hBMSC	Enhanced cell viability		121
Anti–cancer	Trisulfide/PEG–cholesteryl	MCF7 breast cancer cell	Suppressed tumourigenesis	Normalization of COL–1 expression	125
	ADT/AML	HepG2 cell, mice xenograft model	Reduction of tumour size, facilitate magnetic resonance imaging		126

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Recent development of hydrogen sulfide-releasing biomaterials as novel therapies:a narrative review

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