Recent Developments in Nitric Oxide Donors and Delivery for Antimicrobial and Anti-Biofilm Applications
Abstract
:1. Introduction
2. NO Production, Concentration, and Activity
2.1. NO Production, Concentration, and Activity
2.2. NO Mediated Biofilm Formation and Dispersal
2.3. Bacterial Species, Strains, Growth Conditions, and Stage of Biofilm Development Influence Bacterial Response to NO and the Effectiveness of NO Treatment
2.4. Combinations of NO and Antibiotic Treatments
3. Gaseous NO and Other Low Molecular Weight (LMW) NO Donors
3.1. Gaseous NO
3.2. Metal Nitrosyl Complexes
3.3. S-Nitrosothiols
3.4. N-Diazeniumdiolates
3.5. Furoxans
3.6. Photo Responsive/Photoactivated Ruthenium Compounds
3.7. Hybrid-NO Donors
4. Macromolecular NO Donor Scaffolds
General Properties of Macromolecular NO Donor Scaffolds That Can Influence Their Activity
5. Natural Polymer-Based NO-Releasing Scaffolds
5.1. Types of Natural Polymer-Based NO-Releasing Scaffolds
5.2. NO-Releasing Chitosan Oligosaccharides (COS/NO)
5.3. Positive Charge of COS and Association of COS/NO with Bacterial Membranes or Biofilms the Main Driver of Antimicrobial Activity
5.4. Chitosan Gels
5.5. Chitosan-Graft Dendrimers
5.6. NO-Releasing Alginate Scaffolds and Hydrogels
5.7. NO-Releasing Cyclodextrins
6. NO Delivery via Inorganic and Polymeric Nanoparticles and Nanocarriers
6.1. NO-Releasing Silica Nanoparticles
Physical and Surface Properties of NP Affect Their Association with Bacteria and the Activity of Their NO-Releasing NO-NP Counterparts
6.2. NO-Releasing Polymeric Nanoparticles
6.2.1. POEGMA Containing NO-Releasing NPs
6.2.2. PGLA-Based NO-Releasing Nanoparticles
6.2.3. Antibiotic Conjugated or Surface Charge Switchable NO-NPs with Bacteria and Biofilm Targeting Properties
6.2.4. NO-Releasing Materials and Photodynamic and Photothermal Therapy for Antimicrobial Treatment
6.2.5. NO-Releasing Dendrimers and Hyperbranched Polymers
6.3. NO-Releasing Gel, Polymers, and Coatings
7. Conclusions and Future Perspectives
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Sample Availability
Abbreviations
Ag NPs | Silver nanoparticles |
C3D | Cephalosporin-linked diazeniumdiolate NO-donor prodrugs |
CD | Cyclodextrins |
Ce6 | Chlorin e6 |
CF | Cystic fibrosis |
COS-NO | Chitosan oligosaccharides |
CS/NO | NO-releasing chitosan |
ED | 1,2 -epoxy-9-decene |
EPS | Extracellular polysaccharides |
GSH | Gluthathione |
GSNO | S-Nitrosoglutathione |
ICG | Indocyanine green |
IONPs | Iron oxide NPs |
ISMN | Isosorbide mononitrate |
LMW | Low molecular weight |
MDR | Multidrug resistant |
MPs | Microparticles |
MW | Molecular weight |
NIR | Near infrared |
NO | Nitric oxide |
NONOate | Diazeniumdiolates |
NO-NPs | NO-releasing nanoparticles |
NOS | NO synthase |
NPs | Nanoparticles |
PAMAM | Poly(amidoamine) |
PDT | Photodynamic therapy |
PEG | Polyethylene glycol |
PGLA | Poly(lactic-co-glycolic acid) |
PGMA | Poly(glycidyl methacrylate) |
PKA | Poly kanamycin |
PO | Propylene oxide |
POEGMA | Poly (oligoethylene glycol methacrylate) |
Poly(HEMA) | poly(hydroxyethyl methacrylate) |
Poly(SMBA) | poly(sulfobetaine methacrylate) |
PPI | Poly(propylene imine) |
PTFE | Polytetrafluoroethylene |
PTT | Photothermal therapy |
PU | Polyurethane |
PVBA | Poly (vinylbenzaldehyde) |
QS | Quorum sensing |
RNI | Reactive nitrogen intermediates |
RNS | Reactive nitrogen species |
ROI | Reactive oxygen intermediates |
ROS | Reactive oxygen species |
RSNO | S-nitrosothiols |
SNAC | S-nitroso-N-acetylcysteine |
SNAP | S-nitroso-N-acetylpenicillamine |
SNP | Sodium nitroprusside |
SWF | Simulated wound fluid |
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Targeted Delivery of NO to Infection Site | Spontaneous NO Release | |
---|---|---|
High NO concentration |
|
|
Low NO concentration |
|
NO Donor | Concentration of NO Donor/NO | Stains/Test Conditions | Activity | Ref. |
---|---|---|---|---|
Gaseous NO | Continuous 200 ppm NO or intermittent 300 ppm NO | In vitro P. aeruginosa, S. aureus, clinical strains In vivo K. pneumoniae, MDR Klebsiella and S. aureus |
| [56,57] |
Intermittent 160–240 ppm NO | Clinical trials and case studies M. abscessus, E. coli, P. aeruginosa, antibiotic-resistant P. aeruginosa, antibiotic-resistant B. multivoran, S. aureus, and Group B Streptococcus |
| [32,58,59,60,61,62] | |
Metal nitrosyl complexes (e.g., Sodium nitroprusside (SNP)) | 25 µM–100 mM SNP (≈25 nM to 100 µM NO); 5–80 µM SNP (12 h treatment time) | In vitro P. aeruginosa, S. marcescens, V. cholerae, E. coli, F. nucleatum, B. licheniformis, S. epidermidis, C. albicans, and isolates from MBR and RO membrane |
| [6,42,63] |
Photoresponsive ruthenium compounds | µM | In vitro S. epidermidis, P. aeruginosa |
| [64,65] |
S-nitrosothiols (RSNO) (e.g., GSNO, SNAC) | nM–mM | In vitro P. aeruginosa, S. marcescens, V. cholerae, and Keratitis-causing isolates |
| [6,63,66] |
N-diazeniumdiolates (NONOates) | 10 pM–80 µM (Varying treatment duration and dosing regimens) | In vitro Isolates from MBR and RO membrane, S. enterica, E. coli O157:H7, P. aeruginosa, and CF isolates |
| [42,67,68] |
Furoxans | 5–500 µM | In vitro P. aeruginosa |
| [69,70] |
Antimicrobial-NO donor hybrid donors | nM–µM | In vitro P. aeruginosa, S. pneumoniae, Haemophilus influenzae (NTHi), clinical CF isolates of P. aeruginosa, S. aureus, and E. coli In vivo S. aureus |
| [25,26,71,72,73,74,75] |
QS inhibitor—NO hybrid donor | 150 µM | In vitro P. aeruginosa |
| [76] |
Macromolecular NO-Releasing Material | Concentration of NO/NO Donor Used | Stains/Test Conditions | Activity | Ref. |
---|---|---|---|---|
NO-releasing chitosan oligosaccharide (COS/NO) | 0.12–3.1 µmol NO/mL | In vitro Mucoid/non-mucoid/clinical P. aeruginosa, E. coli, and S. aureus |
| [40,113,114,115] |
NO-releasing chitosan gels | Variable depending on design and NO donors used. NO concentrations of ~ nmol NO/mg film or initial NO flux of ~ nmol cm−2 min−1 | In vitro S. aureus, P. aeruginosa, MRSA, L. monocytogenes and E. faecalis In vivo MRSA |
| [13,116,117,118] |
NO-releasing chitosan-dendrimer (CS-PAMAM/NO) | 1–2.5 mg/mL chitosan dendrimer (~1.5 µmol NO/mg) | In vitro E. coli, S. aureus and MRSA In vivo MRSA |
| [21,119] |
NO-releasing alginate | ~ µmol NO/mL for NONOate conjugated alginate | In vitro P. aeruginosa, S. aureus, B. cepacia complex, MRSA, S. mutans, and E. coli |
| [99,120] |
NO-releasing cyclodextrins (NO/CD) | 100–2000 µg/mL NO/CD (~ nmol NO/mL) | In vitro P. aeruginosa |
| [121,122] |
NO-releasing silica NPs (NO-NPs) | ~ µg/mL to mg/mL NO-NPs with varying NO release kinetics and flux | In vitro P. aeruginosa, E. coli, S. aureus, S. epidermidis, S. aureus, A. actinomycetemcomitans, P. gingivalis, and S. mutans |
| [104,123,124,125,126,127] |
NO-releasing silane-based hydrogel nanoparticle platform | Steady state NO in nM range | In vitro MRSA and MSSA S. aureus In vivo MRSA |
| [31,128] |
NO-releasing P(OEGMA) containing polymeric nanoparticles | Variable, dependent on design (see activity for more details) | In vitro P. aeruginosa | Gentamicin-NONOate NPs block copolymer NP
| [54] |
Spherical (S-NO) and worm-like NO-NPs (W-NO)
| [129] | |||
NO releasing polydopamine (PDA)-coated iron oxide NPs
| [105] | |||
Core cross-Linked star polymers
| [23] | |||
NO-releasing polymeric nanoparticles, microparticles, and liposomes | NPs and MPs used in mg/mL range | In vitro S. aureus, MRSA |
| [130,131] |
| [132,133] | |||
Photo-activated NO-releasing polymeric materials | Variable, dependent on design (see activity for more details) | In vitro P. aeruginosa, S. aureus, MRSA, E. coli In vivo S. aureus, MRSA | Self-assembled micellar NPs with hydrophobic antibiotic in core
| [22] |
Surface charge switchable, GSH activated α-CD-Ce6-NO-DA
| [134] | |||
Phototherapeutic nanoplatform AI-MPDA
| [135] | |||
Electrospun nanocomposite membrane (UCNP@PCN@LA-PVDF)
| [136] | |||
PDT-driven NO controllable generation system (Ce6@Arg-ADP)
| [137] | |||
NO-releasing dendrimers | Variable, dependent on design. ~0.69 to 1 µmol NO/mg dendrimer released over 2–4 h in PBS, pH 7.4, 37 °C with max. flux of 2400–15,000 ppb/mg | In vitro P. aeruginosa, S. mutans, S. aureus, S. sanguinis, A. acetinomycetemcomitans, and P. gingivali |
| [100,102,138,139] |
NO-releasing hyperbranched dendrimers | NO storage and NO release ~µmol/mg with half-life ranging from 28 to 80 min depending on design and modifications | In vitro P. gingivalis, A. acetinomycetemcomitans, S. mutansm, S. viscosus, and ex vivo multispecies subgingival biofilms |
| [41,140] |
NO-releasing xerogels and polymer coatings | Variable, dependent on pH, coating, and media (see activity for more details) | In vitro P. aeruginosa | Super-hydrophobic NO-releasing xerogels with fluorinated silane/silica composite topcoat
| [141] |
NO-releasing (poly)acrylonitrile (PAN/NO) polymer
| [142] | |||
NO-releasing coatings on PET and silicone elastomer
| [143] | |||
SNAP-containing Carbosil 2080A polymer (Carbosil-SNAP) with different top coats | In vitro P. aeruginosa, P. mirabilis, S. aureus, E. coli |
| [144,145,146] | |
SNAP-impregnated silicone catheters | NO release ~0.04 nmol/cm2/mL over 60 days or ~ >0.07 nmol/min/cm2 over a month | In vitro P. aeruginosa, P. mirabilis, S. aureus, S. epidermidis |
| [147,148] |
Other NO-releasing surfaces | NO flux in µM range (PBS, pH 7.4, 37 °C) | In vitro P. aeruginosaS. aureus | NO-releasing polydopamine (PDA) coating with PEG grafted onto PDA
| [149] |
NO-releasing titanium surfaces
| [150] | |||
Thiol-functionalized coatings
| [151] | |||
NO release sustained over 15 days at levels >1 nmol/cm2/min and a maximum flux of ~ 3 nmol/cm2/min within <15 min | In vitro S. aureus, S. epidermis, E. faecalis, P. aeruginosa, K. pneumoniae, A. baumannii, and E. coli and relevant MDR isolates, In vivo (Murine subcutaneous infection model) P. aeruginosa, A. baumannii; (Porcine central venous catheterization model) N/A | Precision-structured diblock copolymer brush (H(N)-b-S)
| [24] |
NO Donors/Polymeric Materials | Advantages | Disadvantages |
---|---|---|
NO gas | FDA approved; Direct NO delivery to lung infection sites and surface of wound infections; Side effects easily reversed by stopping NO gas | React with oxygen to give potent pulmonary irritants like NO2 and with hemoglobin to give methemoglobin |
Metal-nitrosyl complexes | Metal-nitrosyl complexes, such as sodium nitroprusside (SNP), is FDA approved and long history of use clinically | Possibility of cyanide toxicity when using SNP for prolonged treatment |
Ru-nitrosyl complexes | Photo-responsive | Relatively new and less well studied for antimicrobial purposes |
S-nitrosothiols (RSNO) | Present endogenously; Some, such as GSNO, have well studied metabolism and low toxicity; NO release can be modulated through various means, including light irradiation; Easily incorporated into polymeric scaffold | Spontaneous release of NO and formation of disulfide bonds in solution; Trans-nitrosylation reaction with other thiol groups present in the body; Multiple mechanisms of degradation by bacteria |
N-diazeniumdiolates (NONOates) | Broad range of reproducible NO release kinetics; Easily incorporated into polymeric materials containing amine moieties by passing NO gas at high pressure; Stable in powder form and in alkaline solutions | Spontaneous NO release in solution under physiological conditions. Not used clinically |
Furoxans | Well-studied NO release with applications in various NO mediated biological processes; Prolong duration of action compared to other NO donors; Thermally stable; May be conjugated to other groups for codelivery of antimicrobials and NO donor | Appears to have other non-NO dependent effects on evaluated bacteria (i.e., P. aeruginosa) that is not well studied or explained with NO release |
Hybrid NO donor | Targeted NO release using antibiotics or antimicrobial peptides; Synergistic effect at eradicating bacteria/biofilm with both targeted NO release and QS inhibition or antimicrobial action | Earlier generations of some hybrid NO donors, such as C3D, require induction of β-lactamase production for activity |
NO-releasing polymeric materials | ||
Chitosan-based NO-releasing materials | Chitosan scaffold is biodegradable, biocompatible and has innate antimicrobial activity; Cationic chitosan promotes association with negatively charged bacterial membranes; Primary amine groups offer a straightforward means of incorporating NO-releasing moieties | In cases like NO-releasing chitosan oligosaccharide (COS/NO), cationic chitosan may improve cohesion of negatively charged biofilms |
Alginate-based NO-releasing materials | Alginate is biodegradable and biocompatible; NO-releasing moieties easily introduced via abundant hydroxyl and carboxylic acid groups; NO release easily tunable by modifying high/low molecular weight alginate used | |
NO-releasing cyclodextrins | Hydrophobic central cavity and hydrophilic exterior could enable delivery of hydrophobic antimicrobial compounds along with NO release | |
NO-releasing silica nanoparticles | Innate antimicrobial activity of nanoparticles. Physiochemical properties, such as shape, sizes, and surface charge can be easily modified to improve NO delivery and bacteria eradication | Cytotoxicity reported in some designs |
NO-releasing polymeric nanoparticles | Specificity and controlled release of NO can be achieved by incorporating photo-responsive groups and surface-charge switchable components; Able to co-deliver antibiotic with NO release to enhance bacterial or biofilm eradication; Other properties, e.g., magnetic field responsive NO-NP, may also be obtained | |
NO-releasing dendrimers | High NO payloads within a single framework; Polymerization of antibiotics enable simultaneous delivery of NO with antibiotic and improve bacteria and biofilm eradication | Cytotoxicity may be associated with higher generation dendrimers and certain chemical modifications/ dendrimers |
NO-releasing gel, polymer, and coatings | NO-releasing surfaces used in blood contacting medical devices may be designed to generate an NO flux representative of endothelial cells; Additional coating along with NO release can extent the anti-fouling lifespan of the material | Leaching of NO may occur depending on the design |
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Poh, W.H.; Rice, S.A. Recent Developments in Nitric Oxide Donors and Delivery for Antimicrobial and Anti-Biofilm Applications. Molecules 2022, 27, 674. https://doi.org/10.3390/molecules27030674
Poh WH, Rice SA. Recent Developments in Nitric Oxide Donors and Delivery for Antimicrobial and Anti-Biofilm Applications. Molecules. 2022; 27(3):674. https://doi.org/10.3390/molecules27030674
Chicago/Turabian StylePoh, Wee Han, and Scott A. Rice. 2022. "Recent Developments in Nitric Oxide Donors and Delivery for Antimicrobial and Anti-Biofilm Applications" Molecules 27, no. 3: 674. https://doi.org/10.3390/molecules27030674