New lipophilic organic nitrates: candidates for chronic skin disease therapy

References

Adler, B.L. and Friedman, A.J. (2015). Nitric oxide therapy for dermatologic disease. Future Sci. OA 1: 37–50.10.4155/fso.15.37Search in Google Scholar PubMed PubMed Central

Ahmed, R., Augustine, R., Chaudhry, M., Akhtar, U.A., Zahid, A.A., Tariq, M., Falahati, M., and Ahmadabd Hasan, I.S.A. (2022). Nitric oxide-releasing biomaterials for promoting wound healing in impaired diabetic wounds: state of the art and recent trends. Biomed. Pharmacother. 149: 112707.10.1016/j.biopha.2022.112707Search in Google Scholar PubMed

Altomare, D.F., Rinaldi, M., Milito, G., Arcanà, F., Spinelli, F., Nardelli, N., Scardigno, D., Pulvirenti-D’Urso, A., Bottini, C., Pescatori, M., et al.. (2000). Glyceryl trinitrate for chronic anal fissure--healing or headache? Results of a multicenter, randomized, placebo-controled, double-blind trial. Dis. Colon Rectum 43: 174–179.10.1007/BF02236977Search in Google Scholar PubMed

Avdeef, A. (2003). Absorption and drug development: solubility, permeability and charge state. Wiley Interscience, Hoboken, New Jersey.10.1002/047145026XSearch in Google Scholar

Baldwin, H., Blanco, D., McKeever, C., Paz, N., Vasquez, Y.N., Quiring, J., Enloe, C., De León, E., and Stasko, N. (2016). Results of a phase 2 efficacy and safety study with SB204, an investigational topical nitric oxide-releasing drug for the treatment of acne vulgaris. J. Clin. Aesthet. Dermatol. 9: 12–18.Search in Google Scholar

Cals-Grierson, M.-M. and Ormerod, A.D. (2004). Nitric oxide function in the skin. Nitric Oxide 10: 179–193.10.1016/j.niox.2004.04.005Search in Google Scholar PubMed

Carapeti, E.A., Kamm, M.A., McDonald, P.J., Chadwick, S.J.D., Melville, D., and Phillips, R.K.S. (1999). Randomised controlled trial shows that glyceryl trinitrate heals anal fissures, higher doses are not more effective, and there is a high recurrence rate. Gut 44: 727–730.10.1136/gut.44.5.727Search in Google Scholar PubMed PubMed Central

Chegaev, K., Lazzarato, L., Tron, G.-C., Marabello, D., Di Stilo, A., Cena, C., Fruttero, R., Gasco, A., Vanthuyne, N., and Roussel, C. (2006). Synthesis, chiral HPLC resolution and configuration assignment of 1-phenylglyceryl trinitrate stereomers. Chirality 18: 430–436.10.1002/chir.20278Search in Google Scholar PubMed

Chegaev, K., Lazzarato, L., Marcarino, P., Di Stilo, A., Fruttero, R., Vanthuyne, N., Roussel, C., and Gasco, A. (2009). Synthesis of some novel organic nitrates and comparative in vitro study of their vasodilator profile. J. Med. Chem. 52: 4020–4025.10.1021/jm9002236Search in Google Scholar PubMed

Cronin, M.T.D., Dearden, J.C., Gupta, R., and Moss, G.P. (1998). An investigation of the mechanism of flux across polydimethylsiloxane membranes by use of quantitative structure-permeability relationships. J. Pharm. Pharmacol. 50: 143–152.10.1111/j.2042-7158.1998.tb06169.xSearch in Google Scholar PubMed

Cronin, M.T.D., Dearden, J.C., Moss, G.P., and Murray-Dichson, G. (1999). Investigation of the mechanism of flux across human skin in vitro by quantitative structure-permeability relationships. Eur. J. Pharmaceut. Sci. 7: 325–330.10.1016/S0928-0987(98)00041-4Search in Google Scholar PubMed

Daiber, A., Wenzel, P., Oelze, M., and Münzel, T. (2008). New insights into bioactivation of organic nitrates, nitrate tolerance and cross-tolerance. Clin. Res. Cardiol. 97: 12–20.10.1007/s00392-007-0588-7Search in Google Scholar PubMed

Daiber, A., Oelze, M., Wenzel, P., Bollmann, F., Pautz, A., and Kleinert, H. (2012). Heme oxygenase-1 induction and organic nitrate therapy: beneficial effects on endothelial dysfunction, nitrate tolerance, and vascular oxidative stress. Int. J. Hypertens. 2012: 842632, https://doi.org/10.1155/2012/842632.Search in Google Scholar PubMed PubMed Central

Dick, I.P. and Scott, R.C. (1992). Pig ear skin as an in-vitro model for human skin permeability. J. Pharm. Pharmacol. 44: 640–645.10.1111/j.2042-7158.1992.tb05485.xSearch in Google Scholar PubMed

Enoch, S. and Leaper, D.J. (2005). Basic science of wound healing. Surgery 23: 37–42.10.1383/surg.23.2.37.60352Search in Google Scholar

Förstermann, U., Closs, E.I., Pollock, J.S., Nakane, M., Schwarz, P., Gath, I., and Kleinert, H. (1994). Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 23: 1121–1131.10.1161/01.HYP.23.6.1121Search in Google Scholar PubMed

Freedman, J.E. and Loscalzo, J. (2003). Nitric oxide and its relationship to thrombotic disorder. J. Thromb. Haemostasis 1: 1183–1188.10.1046/j.1538-7836.2003.00180.xSearch in Google Scholar PubMed

Ganzarolli de Oliveira, M. (2016). S-nitrosothiols as platforms for topical nitric oxide delivery. Basic Clin. Pharmacol. Toxicol. 119: 49–56.10.1111/bcpt.12588Search in Google Scholar PubMed

Geinoz, S., Rey, S., Boss, G., Bunge, A.L., Guy, R.H., Carrupt, P.-A., Reist, M., and Testa, B. (2002). Quantative structure-permeation relationships for solute transport across silicone membranes. Pharm. Res. 19: 1622–1629.10.1023/A:1020745026766Search in Google Scholar PubMed

Geinoz, S., Guy, R.H., Testa, B., and Carrupt, P.-A. (2004). Quantitative structure-permeation relationships (QSPeRs) to predict skin permeation: a critical review. Pharm. Res. 21: 83–92.10.1023/B:PHAM.0000012155.27488.2bSearch in Google Scholar PubMed

Ghaffari, A., Miller, C.C., McMullin, B., and Ghahary, A. (2006). Potential application of gaseous nitric oxide as a topical antimicrobial agent. Nitric Oxide 14: 21–29.10.1016/j.niox.2005.08.003Search in Google Scholar PubMed

Gori, T. (2020). Exogenous NO therapy for the treatment and prevention of atherosclerosis. Int. J. Mol. Sci. 21: 2703–2717.10.3390/ijms21082703Search in Google Scholar PubMed PubMed Central

Heck, D.E., Laskin, D.L., Gardner, C.R., and Laskin, J.D. (1992). Epidermal growth factor suppresses nitric oxide and hydrogen peroxide production by keratinocytes. Potential role for nitric oxide in the regulation of wound healing. J. Biol. Chem. 267: 21277–21280.10.1016/S0021-9258(19)36601-3Search in Google Scholar

Jugdutt, B.I. (1992). Role of nitrates after acute myocardial infarction. Am. J. Med. 70: 82–87.10.1016/0002-9149(92)90598-SSearch in Google Scholar

Karadzovska, D., Brooks, J.D., Monteiro-Riviere, N.A., and Riviere, J.E. (2013). Predicting skin permeability from complex vehicles. Adv. Drug Deliv. Rev. 65: 265–277.10.1016/j.addr.2012.01.019Search in Google Scholar PubMed

Leier, C.V., Bambach, D., Thompson, M.J., Cattaneo, S.M., Goldberg, R.J., and Unverferth, D.V. (1981). Central and regional hemodynamic effects of intravenous isosorbide dinitrate, nitroglycerin and nitroprusside in patients with congestive heart failure. Am. J. Cardiol. 48: 1115–1123.10.1016/0002-9149(81)90329-5Search in Google Scholar PubMed

Malone-Povolny, M.J., Maloney, S.E., and Schoenfisch, M.H. (2019). Nitric oxide therapy for diabetic wound healing. Adv. Healthcare Mater. 8: e1801210.10.1002/adhm.201801210Search in Google Scholar PubMed PubMed Central

Marini, E., Giorgis, M., Leporati, M., Rolando, B., Chegaev, K., Lazzarato, L., Bertinaria, M., Vincenti, M., and Di Stilo, A. (2022). Multitarget antioxidant NO-donor organic nitrates: a novel approach to overcome nitrates tolerance, an ex vivo study. Antioxidants 11: 166–186.10.3390/antiox11010166Search in Google Scholar PubMed PubMed Central

Mizuno, Y., Harada, E., Kugimiya, F., Shono, M., Kusumegi, I., Yoshimura, M., Kinoshita, K., and Yasue, H. (2020). East Asian variant mitochondrial aldehyde dehydrogenase-2 genotype exacerbates nitrate tolerance in patients with coronary spastic angina. Circ. J. 84: 479–486.10.1253/circj.CJ-19-0989Search in Google Scholar PubMed

Münzel, T., Daiber, A., and Mülsch, A. (2005). Explaining the phenomenon of nitrate tolerance. Circ. Res. 97: 618–628.10.1161/01.RES.0000184694.03262.6dSearch in Google Scholar PubMed

Nahir, A.M., Shapira, D., and Sharef, Y. (1986). Double-blind randomized trial of NITRODERM TTS® in the treatment of Raynaud’s phenomenon. Isr. J. Med. Sci. 22: 139–142.Search in Google Scholar

Neupane, R., Boddu, S.H.S., Renukuntla, J., Babu, R.J., and Tiwari, A.K. (2020). Alternatives to biological skin in permeation studies: current trends and possibilities. Pharmaceutics 12: 152–177.10.3390/pharmaceutics12020152Search in Google Scholar PubMed PubMed Central

Omidkhoda, S.F., Razavi, B.M., Imenshahidi, M., Rameshrad, M., and Hosseinzadeh, H. (2020). Evaluation of possible effects of crocin against nitrate tolerance and endothelial dysfunction. Iran. J. Basic Med. Sci. 23: 303–310.Search in Google Scholar

Pecoraro, B., Tutone, M., Hoffman, E., Hutter, V., Almerico, A.M., and Traynor, M. (2019). Predicting skin permeability by means of computational approaches: reliability and caveats in pharmaceutical studies. J. Chem. Inf. Model. 59: 1759–1771.10.1021/acs.jcim.8b00934Search in Google Scholar PubMed

Pulsoni, I., Lubda, M., Aiello, M., Fedi, A., Marzagalli, M., von Hagen, J., and Scaglione, S. (2022). Comparison between Franz diffusion cell and a novel micro-physiological system for in vitro penetration assay using different skin models. SLAS Technol. 27: 161–171.10.1016/j.slast.2021.12.006Search in Google Scholar PubMed

Pyo, S.M. and Maibach, H.I. (2019). Skin metabolism: relevance of skin enzymes for rational drug design. Skin Pharmacol. Physiol. 32: 283–293.10.1159/000501732Search in Google Scholar PubMed

Rolim, W.R., Pieretti, J.C., Renó, D.L.S., Lima, B.A., Nascimento, M.H.M., Ambrosio, F.N., Lombello, C.B., Brocchi, M., de Souza, A.C.S., and Seabra, A.B. (2019). Antimicrobial activity and cytotoxicity to tumor cells of nitric oxide donor and silver nanoparticles containing PVA/PEG films for topical applications. ACS Appl. Mater. Interfaces 11: 6589–6604.10.1021/acsami.8b19021Search in Google Scholar PubMed

Schairer, D.O., Chouake, J.S., Nosanchuk, J.D., and Friedman, A.J. (2012). The potential of nitric oxide releasing therapies as antimicrobial agents. Virulence 3: 271–279.10.4161/viru.20328Search in Google Scholar PubMed PubMed Central

Seabra, A.B., da Silva, R., and de Oliveira, M.G. (2005). Polynitrosatedpolyesters: preparation, characterization, and potential use for topical nitric oxide release. Biomacromolecules 6: 2512–2520.10.1021/bm050216zSearch in Google Scholar PubMed

Sekkat, N. and Guy, R.H. (2001). Biological models to study skin permeation. In: Testa, B., van de Waterbeend, H., Folkers, G., and Guy, R. (Eds.), Pharmakokinetic optimisation in drug research. Wiley-VCH, Wheinheim, pp. 155–172.10.1002/9783906390437.ch10Search in Google Scholar

Snyder, S.H. (1992). Nitric oxide: first in a new class of neurotransmitters. Science 257: 494–496.10.1126/science.1353273Search in Google Scholar PubMed

Suschek, C.V., Feibel, D., von Kohout, M., and Opländer, C. (2022). Enhancement of nitric oxide bioavailability by modulation of cutaneous nitric oxide stores. Biomedicines 10: 2124.10.3390/biomedicines10092124Search in Google Scholar PubMed PubMed Central

Supe, S. and Takudage, P. (2021). Methods for evaluating penetration of drug into the skin: a review. Skin Res. Technol. 27: 299–308.10.1111/srt.12968Search in Google Scholar PubMed

Svensson, C.K. (2009). Biotransformation of drugs in human skin. Drug Metab. Dispos. 37: 247–253.10.1124/dmd.108.024794Search in Google Scholar PubMed

Todo, H. (2017). Transdermal permeation of drugs in various animal species. Pharmaceutics 9: 33–44.10.3390/pharmaceutics9030033Search in Google Scholar PubMed PubMed Central

Urzedo, A.L., Gonçalves, M.C., Nascimento, M.H.M., Lombello, C.B., Nakazato, G., and Seabra, A.B. (2020). Cytotoxicity and antibacterial activity of alginate hydrogel containing nitric oxide donor and silver nanoparticles for topical applications. ACS Biomater. Sci. Eng. 6: 2117–2134.10.1021/acsbiomaterials.9b01685Search in Google Scholar PubMed

Wang, P.G., Xian, M., Tang, X., Wu, X., Wen, Z., Cai, T., and Janczuk, A.J. (2002). Nitric oxide donors: chemical activities and biological applications. Chem. Rev. 102: 1091–1134.10.1021/cr000040lSearch in Google Scholar PubMed

Watson, S.J., Kamm, M.A., Nicholls, R.J., and Phillips, R.K.S. (1996). Topical glyceryl trinitrate in the treatment of chronic anal fissure. Br. J. Surg. 83: 771–775.10.1002/bjs.1800830614Search in Google Scholar PubMed

Weller, R. (2003). Nitric oxide donors and the skin: useful therapeutic agents? Clin. Sci. 105: 533–535.10.1042/CS20030241Search in Google Scholar PubMed

Wigley, F.M. and Flavahan, N.A. (2016). Raynaud’s phenomenon. N. Engl. J. Med. 375: 556–565.10.1056/NEJMra1507638Search in Google Scholar PubMed

Zhang, Y., Tang, K., Chen, B., Zhou, S., Li, N., Liu, C., Yang, J., Lin, R., Zhang, T., and He, W. (2019). A polyethylenimine-based diazeniumdiolate nitric oxide donor accelerates wound healing. Biomater. Sci. 7: 1607–1616.10.1039/C8BM01519HSearch in Google Scholar PubMed

Zhou, X., Zhang, J., Feng, G., Shen, J., Kong, D., and Zhao, Q. (2016). Nitric oxide-releasing biomaterials for biomedical applications. Curr. Med. Chem. 23: 2579–2601.10.2174/0929867323666160729104647Search in Google Scholar PubMed