Hostname: page-component-848d4c4894-sjtt6 Total loading time: 0 Render date: 2024-06-13T12:30:08.711Z Has data issue: false hasContentIssue false

Modulated nitric oxide delivery in three-dimensional biomaterials for vascular functionality

Published online by Cambridge University Press:  19 June 2017

Zuyong Wang
Affiliation:
College of Materials Science and Engineering, Hunan University, Changsha 410082, People's Republic of China
Feng Wen*
Affiliation:
School of Chemical and Biomedical Engineering, Nanyang Technological University, Singapore 637459, Singapore
Rongkai Zhang
Affiliation:
Orthopedics Department, The Fifth Affiliated hospital of Sun Yat-sen University, Sun Yat-sen University, Zhuhai 519000, People's Republic of China
Qinyuan Zhang*
Affiliation:
Singapore Institute of Manufacturing Technology, Singapore 138634, Singapore
*
Address all correspondence to Feng Wen, Qinyuan Zhang at wenfeng@ntu.edu.sg, zqinyuan@gmail.com
Address all correspondence to Feng Wen, Qinyuan Zhang at wenfeng@ntu.edu.sg, zqinyuan@gmail.com
Get access

Abstract

Nitric oxide (NO) acts a pivotal role in regulating various physiological processes of vasodilation, platelet aggregation, and vascular smooth muscle cell mitogenesis and proliferation. This makes NO a promising candidate for the treatment of cardiovascular problems like hypertension and vascular stenosis. However, the high reactivity of NO poses an issue for effective NO delivery. To overcome this limitation, recent developments on three-dimensional (3D) materials have been explored with either physical or chemical incorporation of NO releasing donors, to provide spatiotemporal control over NO-signaling pathways in blood vessels. Here, we offer an overview on the current efforts, and propose future perspectives for precise regulation on NO delivery in advanced 3D materials toward proper vascular functionality.

Type
Biomaterials for 3D Cell Biology Prospective Articles
Copyright
Copyright © Materials Research Society 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

These authors contributed equally to this work.

References

1.Lowenstein, C., Dinerman, J., and Snyder, S.: Nitric oxide: a physiologic messenger. Ann. Intern. Med. 120, 227237 (1994).Google Scholar
2.Seabra, A.B., Justo, G.Z., and Haddad, P.S.: State of the art, challenges and perspectives in the design of nitric oxide-releasing polymeric nanomaterials for biomedical applications. Biotechnol. Adv. 33, 13701379 (2015).Google Scholar
3.Lundberg, J.O., Gladwin, M.T., and Weitzberg, E.: Strategies to increase nitric oxide signalling in cardiovascular disease. Nat. Rev. Drug Discov. 14, 623641 (2015).Google Scholar
4.Garthwaite, J.: Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14, 6067 (1991).Google Scholar
5.Ignarro, L.J.: Heme-dependent activation of soluble guanylate cyclase by nitric oxide: regulation of enzyme activity by porphyrins and metalloporphyrins. Semin. Hematol. 26, 6376 (1989).Google Scholar
6.Hibbs, J.B. Jr.: Synthesis of nitric oxide from L-arginine: a recently discovered pathway induced by cytokines with antitumour and antimicrobial activity. Res. Immunol. 142, 565569 (1991).Google Scholar
7.Azuma, H., Ishikawa, M., and Sekizaki, S.: Endothelium-dependent inhibition of platelet aggregation. Br. J. Pharmacol. 88, 411415 (1986).Google Scholar
8.Leone, A.M., Palmer, R.M., Knowles, R.G., Francis, P.L., Ashton, D.S., and Moncada, S.: Constitutive and inducible nitric oxide synthases incorporate molecular oxygen into both nitric oxide and citrulline. J. Biol. Chem. 266, 2379023795 (1991).Google Scholar
9.Nathan, C.: Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 30513064 (1992).Google Scholar
10.Loscalzo, J. and Welch, G.: Nitric-oxide and its role in the cardiovascular system. Prog. Cardiovasc. Dis. 38, 87104 (1995).Google Scholar
11.Jen, M.C., Serrano, M.C., van Lith, R., and Ameer, G.A.: Polymer-based nitric oxide therapies: recent insights for biomedical applications. Adv. Funct. Mater. 22, 239260 (2012).Google Scholar
12.Straub, A.C., Lohman, A.W., Billaud, M., Johnstone, S.R., Dwyer, S.T., Lee, M.Y., Bortz, P.S., Best, A.K., Columbus, L., and Gaston, B.: Endothelial cell expression of haemoglobin [agr] regulates nitric oxide signalling. Nature 491, 473477 (2012).Google Scholar
13.Wang, Z., Teoh, S.H., Hong, M., Luo, F., Teo, E.Y., Chan, J.K.Y., and Thian, E.S.: Dual-microstructured porous, anisotropic film for biomimicking of endothelial basement membrane. ACS Appl. Mater. Interfaces 7, 1344513456 (2015).Google Scholar
14.Wang, Z., Du, Z., Chan, J.K.Y., Teoh, S.H., Thian, E.S., and Hong, M.: Direct laser microperforation of bioresponsive surface-patterned films with through-hole arrays for vascular tissue-engineering application. ACS Biomater. Sci. Eng. 1, 12391249 (2015).Google Scholar
15.Butler, A.R. and Williams, D.L.H.: The physiological role of nitric oxide. Chem. Soc. Rev. 22, 233241 (1993).Google Scholar
16.Gladwin, M.T. and Kim-Shapiro, D.B.: Vascular biology: nitric oxide caught in traffic. Nature 491, 344345 (2012).Google Scholar
17.Hall, C.N. and Garthwaite, J.: What is the real physiological NO concentration in vivo? Nitric Oxide 21, 92103 (2009).Google Scholar
18.Brookes, P.S., Salinas, E.P., Darley-Usmar, K., Eiserich, J.P., Freeman, B.A., Darley-Usmar, V.M., and Anderson, P.G.: Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J. Biol. Chem. 275, 2047420479 (2000).Google Scholar
19.Gow, A.J., Farkouh, C.R., Munson, D.A., Posencheg, M.A., and Ischiropoulos, H.: Biological significance of nitric oxide-mediated protein modifications. Am. J. Physiol.: Lung Cell. Mol. Physiol. 287, L262L268 (2004).Google Scholar
20.Kaster, M.P., Rosa, A.O., Santos, A.R., and Rodrigues, A.L.: Involvement of nitric oxide-cGMP pathway in the antidepressant-like effects of adenosine in the forced swimming test. Int. J. Neuropsychopharmacol. 8, 601606 (2005).Google Scholar
21.Schulz, R. and Triggle, C.R.: Role of NO in vascular smooth muscle and cardiac muscle function. Trends Pharmacol. Sci. 15, 255259 (1994).Google Scholar
22.Kim, Y.M., Talanian, R.V., and Billiar, T.R.: Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272, 3113831148 (1997).Google Scholar
23.Kibbe, M.R., Li, J., Nie, S., Watkins, S.C., Lizonova, A., Kovesdi, I., Simmons, R.L., Billiar, T.R., and Tzeng, E.: Inducible nitric oxide synthase (iNOS) expression upregulates p21 and inhibits vascular smooth muscle cell proliferation through p42/44 mitogen-activated protein kinase activation and independent of p53 and cyclic guanosine monophosphate. J. Vasc. Surg. 31, 12141228 (2000).Google Scholar
24.Sarkar, R. and Webb, R.C.: Does nitric oxide regulate smooth muscle cell proliferation? A critical appraisal. J. Vasc. Res. 35, 135142 (1998).Google Scholar
25.Jeremy, J.Y., Rowe, D., Emsley, A.M., and Newby, A.C.: Nitric oxide and the proliferation of vascular smooth muscle cells. Cardiovasc. Res. 43, 580594 (1999).Google Scholar
26.Janero, D.R. and Ewing, J.F.: Nitric oxide and postangioplasty restenosis: pathological correlates and therapeutic potential. Free Radical Biol. Med. 29, 11991221 (2000).Google Scholar
27.Loscalzo, J.: Nitric oxide and restenosis. Clin. Appl. Thromb. Hemost. 2, 710 (1996).Google Scholar
28.Cannon, R.O. III: Role of nitric oxide in cardiovascular disease: focus on the endothelium. Clin. Chem. 44, 18091819 (1998).Google Scholar
29.Lafont, A., Guzman, L.A., Whitlow, P.L., Goormastic, M., Cornhill, J.F., and Chisolm, G.M.: Restenosis after experimental angioplasty. Intimal, medial, and adventitial changes associated with constrictive remodeling. Circ. Res. 76, 9961002 (1995).Google Scholar
30.Stemerman, M.B. and Ross, R.: Experimental arteriosclerosis. I. Fibrous plaque formation in primates, an electron microscopic study. J. Exp. Med. 136, 769789 (1972).Google Scholar
31.Garrel, C. and Fontecave, M.: Nitric oxide: chemistry and biology. In Analysis of Free Radicals in Biological Systems, edited by Favier, A.E., Cadet, J., Kalyanaraman, B., Fontecave, M., and Pierre, J.L. (Birkhäuser Basel, Basel, 1995), pp. 2135.Google Scholar
32.Nossaman, V.E., Nossaman, B.D., and Kadowitz, P.J.: Nitrates and nitrites in the treatment of ischemic cardiac disease. Cardiol. Rev. 18, 190197 (2010).Google Scholar
33.Omar, S.A., Artime, E., and Webb, A.J.: A comparison of organic and inorganic nitrates/nitrites. Nitric Oxide 26, 229240 (2012).Google Scholar
34.King, S.B.: Mechanisms and novel directions in the biological applications of nitric oxide donors. Free Radical Biol. Med. 37, 735736 (2004).Google Scholar
35.Jerie, P.: Milestones of cardiovascular therapy. III. Nitroglycerin. Cas. Lek. Cesk. 146, 533537 (2007).Google Scholar
36.Gori, T. and Parker, J.D.: Nitrate tolerance—a unifying hypothesis. Circulation 106, 25102513 (2002).Google Scholar
37.Munzel, T., Li, H., Mollnau, H., Hink, U., Matheis, E., Hartmann, M., Oelze, M., Skatchkov, M., Warnholtz, A., Duncker, L., Meinertz, T., and Forstermann, U.: Effects of long-term nitroglycerin treatment on endothelial nitric oxide synthase (NOS III) gene expression, NOS III-mediated superoxide production, and vascular NO bioavailability. Circ. Res. 86, E7E12 (2000).Google Scholar
38.Fung, H.L.: Clinical pharmacology of organic nitrates. Am. J. Cardiol. 72, C9C15 (1993).Google Scholar
39.Miller, M.R. and Megson, I.L.: Recent developments in nitric oxide donor drugs. Br. J. Pharmacol. 151, 305321 (2007).Google Scholar
40.Grossi, L. and D'Angelo, S.: Sodium nitroprusside: mechanism of NO release mediated by sulfhydryl-containing molecules. J. Med. Chem. 48, 26222626 (2005).Google Scholar
41.Butler, A.R. and Glidewell, C.: Recent chemical studies of sodium nitroprusside relevant to its hypotensive action. Chem. Soc. Rev. 16, 361380 (1987).Google Scholar
42.Megson, I.L.: Nitric oxide donor drugs. Drugs Future 25, 701715 (2000).Google Scholar
43.Feelisch, M., Ostrowski, J., and Noack, E.: On the mechanism of NO release from sydnonimines. J. Cardiovasc. Pharmacol. 14(Suppl. 11), S13S22 (1989).Google Scholar
44.Reden, J.: Molsidomine. Blood Vessels 27, 282294 (1990).Google Scholar
45.Megson, I.L. and Webb, D.J.: Nitric oxide donor drugs: current status and future trends. Expert Opin. Invest. Drugs 11, 587601 (2002).Google Scholar
46.King, S.B.: C-nitroso compounds, oximes, N-hydroxyguanidines and N-hydroxyureas. In Nitric Oxide Donors, edited by Wang, P.G., Cai, T.B. and Taniguchi, N. (Wiley-VCH Verlag GmbH & Co. KGaA2005, Weinheim, FRG), pp. 177199.Google Scholar
47.Chakrapani, H., Bartberger, M.D., and Toone, E.J.: C-nitroso donors of nitric oxide. J. Org. Chem. 74, 14501453 (2009).Google Scholar
48.Gowenlock, B.G. and Richter-Addo, G.B.: Preparations of C-nitroso compounds. Chem. Rev. 104, 33153340 (2004).Google Scholar
49.Lam, C.F., Sviri, S., Ilett, K.F., and van Heerden, P.V.: Inhaled diazeniumdiolates (NONOates) as selective pulmonary vasodilators. Expert Opin. Invest. Drugs 11, 897909 (2002).Google Scholar
50.Maragos, C.M., Morley, D., Wink, D.A., Dunams, T.M., Saavedra, J.E., Hoffman, A., Bove, A.A., Isaac, L., Hrabie, J.A., and Keefer, L.K.: Complexes of .NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects. J. Med. Chem. 34, 32423247 (1991).Google Scholar
51.Fitzhugh, A.L., and Keefer, L.K.: Diazeniumdiolates: pro- and antioxidant applications of the “NONOates”. Free Radical Biol. Med. 28, 14631469 (2000).Google Scholar
52.Mowery, K.A., Schoenfisch, M.H., Saavedra, J.E., Keefer, L.K., and Meyerhoff, M.E.: Preparation and characterization of hydrophobic polymeric films that are thromboresistant via nitric oxide release. Biomaterials 21, 921 (2000).Google Scholar
53.Al-Sa'doni, H. and Ferro, A.: S-nitrosothiols: a class of nitric oxide-donor drugs. Clin. Sci. 98, 507520 (2000).Google Scholar
54.Holmes, A.J. and Williams, D.L.H.: Reaction of ascorbic acid with S-nitrosothiols: clear evidence for two distinct reaction pathways. J. Chem. Soc., Perkin Trans. 2, 16391644 (2000).Google Scholar
55.Friedman, A. and Friedman, J.: New biomaterials for the sustained release of nitric oxide: past, present and future. Expert Opin. Drug Delivery 6, 11131122 (2009).Google Scholar
56.Hanspal, I.S., Magid, K.S., Webb, D.J., and Megson, I.L.: The effect of oxidative stress on endothelium-dependent and nitric oxide donor-induced relaxation: implications for nitrate tolerance. Nitric Oxide 6, 263270 (2002).Google Scholar
57.Ramsay, B., Radomski, M., De Belder, A., Martin, J.F., and Lopez-Jaramillo, P.: Systemic effects of S-nitroso-glutathione in the human following intravenous infusion. Br. J. Clin. Pharmacol. 40, 101102 (1995).Google Scholar
58.Al-Sa'doni, H.H., Khan, I.Y., Poston, L., Fisher, I., and Ferro, A.: A novel family of S-nitrosothiols: chemical synthesis and biological actions. Nitric Oxide 4, 550560 (2000).Google Scholar
59.Roy, B., du Moulinet d'Hardemare, A., and Fontecave, M.: New thionitrites: synthesis, stability, and nitric oxide generation. J. Org. Chem. 59, 70197026 (1994).Google Scholar
60.Hrabie, J.A. and Keefer, L.K.: Chemistry of the nitric oxide-releasing diazeniumdiolate (“nitrosohydroxylamine”) functional group and its oxygen-substituted derivatives. Chem. Rev. 102, 11351154 (2002).Google Scholar
61.Mowery, K.A. and Meyerhoff, M.E.: The transport of nitric oxide through various polymeric matrices. Polymer 40, 62036207 (1999).Google Scholar
62.Batchelor, M.M., Reoma, S.L., Fleser, P.S., Nuthakki, V.K., Callahan, R.E., Shanley, C.J., Politis, J.K., Elmore, J., Merz, S.I., and Meyerhoff, M.E.: More lipophilic dialkyldiamine-based diazeniumdiolates: synthesis, characterization, and application in preparing thromboresistant nitric oxide release polymeric coatings. J. Med. Chem. 46, 51535161 (2003).Google Scholar
63.Bohl, K. and West, J.: Nitric oxide-generating polymers reduce platelet adhesion and smooth muscle cell proliferation. Biomaterials 21, 22732278 (2000).Google Scholar
64.Saavedra, J.E., Southan, G.J., Davies, K.M., Lundell, A., Markou, C., Hanson, S.R., Adrie, C., Hurford, W.E., Zapol, W.M., and Keefer, L.K.: Localizing antithrombotic and vasodilatory activity with a novel, ultrafast nitric oxide donor. J. Med. Chem. 39, 43614365 (1996).Google Scholar
65.Smith, D.J., Chakravarthy, D., Pulfer, S., Simmons, M.L., Hrabie, J.A., Citro, M.L., Saavedra, J.E., Davies, K.M., Hutsell, T.C., Mooradian, D.L., Hanson, S.R., and Keefer, L.K.: Nitric oxide-releasing polymers containing the [N(O)NO]- group. J. Med. Chem. 39, 11481156 (1996).Google Scholar
66.Seabra, A.B. and de Oliveira, M.G.: Poly(vinyl alcohol) and poly(vinyl pyrrolidone) blended films for local nitric oxide release. Biomaterials 25, 37733782 (2004).Google Scholar
67.Seabra, A.B., Da Rocha, L.L., Eberlin, M.N., and De Oliveira, M.G.: Solid films of blended poly(vinyl alcohol)/poly(vinyl pyrrolidone) for topical S-nitrosoglutathione and nitric oxide release. J. Pharm. Sci. 94, 9941003 (2005).Google Scholar
68.Saavedra, J.E., Booth, M.N., Hrabie, J.A., Davies, K.M., and Keefer, L.K.: Piperazine as a linker for incorporating the nitric oxide-releasing diazeniumdiolate group into other biomedically relevant functional molecules. J. Org. Chem. 64, 51245131 (1999).Google Scholar
69.de Oliveira, F.G., da Silva, R., Seabra, A.B., and de Oliveira, M.G.: Nitric oxide functionalized polyesters improve hemocompatibility of blood contacting surfaces. Nitric Oxide 19, S66S66 (2008).Google Scholar
70.Li, Y. and Lee, P.I.: Controlled nitric oxide delivery platform based on S-nitrosothiol conjugated interpolymer complexes for diabetic wound healing. Mol. Pharmaceutics. 7, 254266 (2010).Google Scholar
71.Shishido, S.L.M., Seabra, A.B., Loh, W., and Ganzarolli de Oliveira, M.: Thermal and photochemical nitric oxide release from S-nitrosothiols incorporated in Pluronic F127 gel: potential uses for local and controlled nitric oxide release. Biomaterials 24, 35433553 (2003).Google Scholar
72.Seabra, A.B., Fitzpatrick, A., Paul, J., De Oliveira, M.G., and Weller, R.: Topically applied S-nitrosothiol-containing hydrogels as experimental and pharmacological nitric oxide donors in human skin. Br. J. Dermatol. 151, 977983 (2004).Google Scholar
73.Simoes, M.M. and de Oliveira, M.G.: Poly(vinyl alcohol) films for topical delivery of S-nitrosoglutathione: effect of freezing-thawing on the diffusion properties. J. Biomed. Mater. Res. B 93, 416424 (2010).Google Scholar
74.Masters, K.S., Leibovich, S.J., Belem, P., West, J.L., and Poole-Warren, L.A.: Effects of nitric oxide releasing poly(vinyl alcohol) hydrogel dressings on dermal wound healing in diabetic mice. Wound Repair Regen. 10, 286294 (2002).Google Scholar
75.Lipke, E.A. and West, J.L.: Localized delivery of nitric oxide from hydrogels inhibits neointima formation in a rat carotid balloon injury model. Acta Biomater. 1, 597606 (2005).Google Scholar
76.Masters, K.S., Lipke, E.A., Rice, E.E., Liel, M.S., Myler, H.A., Zygourakis, C., Tulis, D.A., and West, J.L.: Nitric oxide-generating hydrogels inhibit neointima formation. J. Biomater. Sci., Polym. Ed. 16, 659672 (2005).Google Scholar
77.Taite, L. and West, J.: Sustained delivery of nitric oxide from poly(ethylene glycol) hydrogels enhances endothelialization in a rat carotid balloon injury model. Cardiovasc. Eng. Tech. 2, 113123 (2011).Google Scholar
78.Kim, J., Lee, Y., Singha, K., Kim, H.W., Shin, J.H., Jo, S., Han, D.K., and Kim, W.J.: NONOates--polyethylenimine hydrogel for controlled nitric oxide release and cell proliferation modulation. Bioconjugate Chem. 22, 10311038 (2011).Google Scholar
79.Marxer, S.M., Rothrock, A.R., Nablo, B.J., Robbins, M.E., and Schoenfisch, M.H.: Preparation of nitric oxide (NO)-releasing sol−gels for biomaterial applications. Chem. Mat. 15, 41934199 (2003).Google Scholar
80.Forslund, T. and Sundqvist, T.: Nitric oxide-releasing particles inhibit phagocytosis in human neutrophils. Biochem. Biophys. Res. Commun. 233, 492495 (1997).Google Scholar
81.Reynolds, M.M., Frost, M.C., and Meyerhoff, M.E.: Nitric oxide-releasing hydrophobic polymers: preparation, characterization, and potential biomedical applications. Free Radical Biol. Med. 37, 926936 (2004).Google Scholar
82.Frost, M.C. and Meyerhoff, M.E.: Synthesis, characterization, and controlled nitric oxide release from S-nitrosothiol-derivatized fumed silica polymer filler particles. J. Biomed. Mater. Res., Part A 72A, 409419 (2005).Google Scholar
83.Zhang, H.P., Annich, G.M., Miskulin, J., Stankiewicz, K., Osterholzer, K., Merz, S.I., Bartlett, R.H., and Meyerhoff, M.E.: Nitric oxide-releasing fumed silica particles: synthesis, characterization, and biomedical application. J. Am. Chem. Soc. 125, 50155024 (2003).Google Scholar
84.Vaughn, M.W., Kuo, L., and Liao, J.C.: Effective diffusion distance of nitric oxide in the microcirculation. Am. J. Physiol. 274, H1705H1714 (1998).Google Scholar
85.Carpenter, A.W., Slomberg, D.L., Rao, K.S., and Schoenfisch, M.H.: Influence of scaffold size on bactericidal activity of nitric oxide-releasing silica nanoparticles. ACS Nano 5, 72357244 (2011).Google Scholar
86.Shin, J.H. and Schoenfisch, M.H.: Inorganic/organic hybrid silica nanoparticles as a nitric oxide delivery scaffold. Chem. Mater. 20, 239249 (2007).Google Scholar
87.Zhang, Q., Wang, Z., Wen, F., Ren, L., Li, J., Teoh, S.H., and Thian, E.S.: Gelatin-siloxane nanoparticles to deliver nitric oxide for vascular cell regulation: synthesis, cytocompatibility, and cellular responses. J. Biomed. Mater. Res. A 103, 929938 (2015).Google Scholar
88.Rothrock, A.R., Donkers, R.L., and Schoenfisch, M.H.: Synthesis of nitric oxide-releasing gold nanoparticles. J. Am. Chem. Soc. 127, 93629363 (2005).Google Scholar
89.Polizzi, M.A., Stasko, N.A., and Schoenfisch, M.H.: Water-soluble nitric oxide-releasing gold nanoparticles. Langmuir 23, 49384943 (2007).Google Scholar
90.Alkilany, A.M. and Murphy, C.J.: Toxicity and cellular uptake of gold nanoparticles: what we have learned so far? J. Nanopart. Res. 12, 23132333 (2010).Google Scholar
91.Gref, R., Minamitake, Y., Peracchia, M.T., Trubetskoy, V., Torchilin, V., and Langer, R.: Biodegradable long-circulating polymeric nanospheres. Science 263, 16001603 (1994).Google Scholar
92.Kumar, V., Hong, S.Y., Maciag, A.E., Saavedra, J.E., Adamson, D.H., Prud'homme, R.K., Keefer, L.K., and Chakrapani, H.: Stabilization of the nitric oxide (NO) prodrugs and anticancer leads, PABA/NO and Double JS-K, through incorporation into PEG-protected nanoparticles. Mol. Pharm. 7, 291298 (2010).Google Scholar
93.Yoo, J.W., Lee, J.S., and Lee, C.H.: Characterization of nitric oxide-releasing microparticles for the mucosal delivery. J. Biomed. Mater. Res. A 92, 12331243 (2010).Google Scholar
94.Friedman, A.J., Han, G., Navati, M.S., Chacko, M., Gunther, L., Alfieri, A., and Friedman, J.M.: Sustained release nitric oxide releasing nanoparticles: characterization of a novel delivery platform based on nitrite containing hydrogel/glass composites. Nitric Oxide 19, 1220 (2008).Google Scholar
95.Martinez, L.R., Han, G., Chacko, M., Mihu, M.R., Jacobson, M., Gialanella, P., Friedman, A.J., Nosanchuk, J.D., and Friedman, J.M.: Antimicrobial and healing efficacy of sustained release nitric oxide nanoparticles against Staphylococcus aureus skin infection. J. Invest. Dermatol. 129, 24632469 (2009).Google Scholar
96.Cabrales, P., Han, G., Roche, C., Nacharaju, P., Friedman, A.J., and Friedman, J.M.: Sustained release nitric oxide from long-lived circulating nanoparticles. Free Radical Biol. Med. 49, 530538 (2010).Google Scholar
97.Tong, S.Y., Wang, Z., Lim, P.N., Wang, W., and San Thian, E.: Uniformly-dispersed nanohydroxapatite-reinforced poly(ε-caprolactone) composite films for tendon tissue engineering application. Mater. Sci. Eng. C 70, 11491155 (2017).Google Scholar
98.Wang, Z., Wen, F., Lim, P.N., Zhang, Q., Konishi, T., Wang, D., Teoh, S.H., and Thian, E.S.: Nanomaterial scaffolds to regenerate musculoskeletal tissue: signals from within for neovessel formation. Drug Discov. Today (2017). doi: doi.org/10.1016/j.drudis.2017.03.010.Google Scholar
99.Wang, Z., Teo, E., Chong, M., Zhang, Q., Lim, J., Zhang, Z., Hong, M., Thian, E.S., Chan, J., and Teoh, S.H.: Biomimetic three-dimensional anisotropic geometries by uniaxial stretch of poly (ε-caprolactone) films for mesenchymal stem cell proliferation, alignment, and myogenic differentiation. Tissue Eng. C 19, 538549 (2013).Google Scholar
100.Wang, Z., Teoh, S.H., Johana, N.B., Chong, M., Teo, E., Hong, M., Chan, J., and Thian, E.S.: Enhancing mesenchymal stem cell response using uniaxially stretched poly(ε-caprolactone) film micropatterns for vascular tissue engineering application. J. Mater. Chem. B 2, 58985909 (2014).Google Scholar
101.Hoo, S.P., Sarvi, F., Li, W.H., Chan, P.P., and Yue, Z.: Thermoresponsive cellulosic hydrogels with cell-releasing behavior. ACS Appl. Mater. Interfaces 5, 55925600 (2013).Google Scholar
102.Chen, Y., Yue, Z., Moulton, S.E., Hayes, P., Cook, M.J., and Wallace, G.G.: A simple and versatile method for microencapsulation of anti-epileptic drugs for focal therapy of epilepsy. J. Mater. Chem. B 3, 72557261 (2015).Google Scholar
103.Jayasinghe, S.N.: Cell electrospinning: a novel tool for functionalising fibres, scaffolds and membranes with living cells and other advanced materials for regenerative biology and medicine. Analyst 138, 22152223 (2013).Google Scholar
104.Townsend-Nicholson, A. and Jayasinghe, S.N.: Cell electrospinning: a unique biotechnique for encapsulating living organisms for generating active biological microthreads/scaffolds. Biomacromolecules 7, 33643369 (2006).Google Scholar